Remote Ischemic Post-Conditioning Therapy is Protective in Mouse Model of Traumatic Optic Neuropathy.
Adenylate Kinase
/ biosynthesis
Animals
Blood-Retinal Barrier
Caspase 3
/ biosynthesis
Cell Death
Eye Proteins
/ biosynthesis
Hindlimb
/ blood supply
Interleukin-10
/ blood
Ischemia
/ physiopathology
Ischemic Postconditioning
Male
Mice
Mice, Inbred C57BL
Microglia
/ physiology
Models, Animal
NADPH Oxidase 2
/ analysis
Neuroinflammatory Diseases
/ etiology
Optic Nerve Injuries
/ therapy
Oxidative Stress
Retinal Ganglion Cells
/ pathology
Superoxides
/ analysis
Transcription Factor Brn-3A
/ biosynthesis
Tumor Necrosis Factor-alpha
/ blood
Tyrosine
/ analogs & derivatives
Inflammation
Optic nerve injury
Oxidative stress
Remote-limb ischemic conditioning (RIC)
Tight junction
Journal
Neuromolecular medicine
ISSN: 1559-1174
Titre abrégé: Neuromolecular Med
Pays: United States
ID NLM: 101135365
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
26
09
2020
accepted:
30
10
2020
pubmed:
14
11
2020
medline:
17
3
2022
entrez:
13
11
2020
Statut:
ppublish
Résumé
Traumatic optic neuropathy (TON) is characterized by visual dysfunction after indirect or direct injury to the optic nerve following blunt head trauma. TON is associated with increased oxidative stress and inflammation resulting in retinal ganglion cell (RGC) death. Remote ischemic post-conditioning (RIC) has been shown to enhance endogenous protective mechanisms in diverse disease models including stroke, vascular cognitive impairment (VCI), retinal injury and optic nerve injury. However, the protective mechanisms underlying the improvement of retinal function and RGC survival after RIC treatment remain unclear. Here, we hypothesized that RIC therapy may be protective following TON by preventing RGC death, oxidative insult and inflammation in the mouse retina. To carry out the study, mice were divided in three different groups (Control, TON and TON + RIC). We harvested retinal tissue 5 days after TON induction for western blotting and histochemical analysis. We observed increased TON-induced retinal cell death compared with controls by cleaved caspase-3 immunohistochemistry. Furthermore, the TON cohort demonstrated increased TUNEL positive cells which were significantly attenuated by RIC. Immunofluorescence data showed that oxidative stress markers dihydroethidium (DHE), NOX-2 and nitrotyrosine expression were elevated in the TON group relative to controls and RIC therapy significantly reduced the expression level of these markers. Next, we found that the proinflammatory cytokine TNF-α was increased and anti-inflammatory IL-10 was decreased in plasma of TON animals, and RIC therapy reversed this expression level. Interestingly, western blotting of retinal tissue showed that RGC marker Brn3a and tight junction proteins (ZO-1 and Occludin), and AMPKα1 expression were downregulated in the TON group compared to controls. However, RIC significantly increased the expression levels of these proteins. Together these data suggest that RIC therapy activates endogenous protective mechanisms which may attenuate TON-induced oxidative stress and inflammation, and improves BRB integrity.
Identifiants
pubmed: 33185833
doi: 10.1007/s12017-020-08631-1
pii: 10.1007/s12017-020-08631-1
doi:
Substances chimiques
Eye Proteins
0
IL10 protein, mouse
0
Pou4f1 protein, mouse
0
Transcription Factor Brn-3A
0
Tumor Necrosis Factor-alpha
0
Superoxides
11062-77-4
Interleukin-10
130068-27-8
3-nitrotyrosine
3604-79-3
Tyrosine
42HK56048U
Cybb protein, mouse
EC 1.6.3.-
NADPH Oxidase 2
EC 1.6.3.-
Adenylate Kinase
EC 2.7.4.3
Casp3 protein, mouse
EC 3.4.22.-
Caspase 3
EC 3.4.22.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
371-382Informations de copyright
© 2020. Springer Science+Business Media, LLC, part of Springer Nature.
Références
Ahmad, S., Elsherbiny, N. M., Bhatia, K., Elsherbini, A. M., Fulzele, S., & Liou, G. I. (2014). Inhibition of adenosine kinase attenuates inflammation and neurotoxicity in traumatic optic neuropathy. Journal of Neuroimmunology, 277, 96–104.
pubmed: 25457840
doi: 10.1016/j.jneuroim.2014.10.006
pmcid: 25457840
Ahmad, S., Fatteh, N., El-Sherbiny, N. M., Naime, M., Ibrahim, A. S., El-Sherbini, A. M., et al. (2013). Potential role of A2A adenosine receptor in traumatic optic neuropathy. Journal of Neuroimmunology, 264, 54–64.
pubmed: 24090652
doi: 10.1016/j.jneuroim.2013.09.015
pmcid: 24090652
Belforte, N., Sande, P. H., de Zavalia, N., Fernandez, D. C., Silberman, D. M., Chianelli, M. S., & Rosenstein, R. E. (2011). Ischemic tolerance protects the rat retina from glaucomatous damage. PLoS ONE, 6, e23763.
pubmed: 21887313
pmcid: 3161053
doi: 10.1371/journal.pone.0023763
Bernardo-Colon, A., Vest, V., Clark, A., Cooper, M. L., Calkins, D. J., Harrison, F. E., & Rex, T. S. (2018). Antioxidants prevent inflammation and preserve the optic projection and visual function in experimental neurotrauma. Cell Death and Diseases, 9, 1097.
doi: 10.1038/s41419-018-1061-4
Biousse, V., & Newman, N. J. (2016). Diagnosis and clinical features of common optic neuropathies. The Lancet Neurology, 15, 1355–1367.
pubmed: 27839652
doi: 10.1016/S1474-4422(16)30237-X
pmcid: 27839652
Botker, H. E., Kharbanda, R., Schmidt, M. R., Bottcher, M., Kaltoft, A. K., Terkelsen, C. J., et al. (2010). Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. The Lancet, 375, 727–734.
doi: 10.1016/S0140-6736(09)62001-8
Brandli, A., Johnstone, D. M., & Stone, J. (2016). Remote ischemic preconditioning protects retinal photoreceptors: Evidence from a rat model of light-induced photoreceptor degeneration. Investigative Ophthalmology & Visual Science, 57, 5302–5313.
doi: 10.1167/iovs.16-19361
Chaon, B. C., & Lee, M. S. (2015). Is there treatment for traumatic optic neuropathy? Current Opinion in Ophthalmology, 26, 445–449.
pubmed: 26448040
doi: 10.1097/ICU.0000000000000198
pmcid: 26448040
Chen, L., Wang, J., You, Q., He, S., Meng, Q., Gao, J., et al. (2018). Activating AMPK to restore tight junction assembly in intestinal epithelium and to attenuate experimental colitis by metformin. Frontiers in Pharmacology, 9, 761.
pubmed: 30061832
pmcid: 6054982
doi: 10.3389/fphar.2018.00761
Dreixler, J. C., Shaikh, A. R., Alexander, M., Savoie, B., & Roth, S. (2010). Post-ischemic conditioning in the rat retina is dependent upon ischemia duration and is not additive with ischemic pre-conditioning. Experimental Eye Research, 91, 844–852.
pubmed: 20599964
pmcid: 2976837
doi: 10.1016/j.exer.2010.06.015
England, T. J., Hedstrom, A., O’Sullivan, S., Donnelly, R., Barrett, D. A., Sarmad, S., et al. (2017). RECAST (Remote ischemic conditioning after stroke trial): A pilot randomized placebo controlled phase II trial in acute ischemic stroke. Stroke, 48, 1412–1415.
pubmed: 28265014
doi: 10.1161/STROKEAHA.116.016429
Fernandez, D. C., Bordone, M. P., Chianelli, M. S., & Rosenstein, R. E. (2009). Retinal neuroprotection against ischemia-reperfusion damage induced by postconditioning. Investigative Ophthalmology & Visual Science, 50, 3922–3930.
doi: 10.1167/iovs.08-3344
Fernandez, D. C., Sande, P. H., Chianelli, M. S., Aldana Marcos, H. J., & Rosenstein, R. E. (2011). Induction of ischemic tolerance protects the retina from diabetic retinopathy. American Journal of Pathology, 178, 2264–2274.
doi: 10.1016/j.ajpath.2011.01.040
Gonzalez, N. R., Connolly, M., Dusick, J. R., Bhakta, H., & Vespa, P. (2014). Phase I clinical trial for the feasibility and safety of remote ischemic conditioning for aneurysmal subarachnoid hemorrhage. Neurosurgery, 75, 590–598. (discussion 598).
pubmed: 25072112
doi: 10.1227/NEU.0000000000000514
Grinblat, G. A., Khan, R. S., Dine, K., Wessel, H., Brown, L., & Shindler, K. S. (2018). RGC neuroprotection following optic nerve trauma mediated by intranasal delivery of amnion cell secretome. Investigative Ophthalmology & Visual Science, 59, 2470–2477.
doi: 10.1167/iovs.18-24096
Guragain, D., Gurung, P., Chang, J. H., Katila, N., Chang, H. W., Jeong, B. S., et al. (2020). AMPK is essential for IL-10 expression and for maintaining balance between inflammatory and cytoprotective signaling. Biochimica et Biophysica Acta - General Subjects, 1864, 129631.
pubmed: 32418902
doi: 10.1016/j.bbagen.2020.129631
Hess, D. C., Blauenfeldt, R. A., Andersen, G., Hougaard, K. D., Hoda, M. N., Ding, Y., & Ji, X. (2015). Remote ischaemic conditioning-A new paradigm of self-protection in the brain. Nature Reviews Neurology, 11, 698–710.
pubmed: 26585977
doi: 10.1038/nrneurol.2015.223
Hines-Beard, J., Marchetta, J., Gordon, S., Chaum, E., Geisert, E. E., & Rex, T. S. (2012). A mouse model of ocular blast injury that induces closed globe anterior and posterior pole damage. Experimental Eye Research, 99, 63–70.
pubmed: 22504073
pmcid: 3922065
doi: 10.1016/j.exer.2012.03.013
Hoda, M. N., Siddiqui, S., Herberg, S., Periyasamy-Thandavan, S., Bhatia, K., Hafez, S. S., et al. (2012). Remote ischemic perconditioning is effective alone and in combination with intravenous tissue-type plasminogen activator in murine model of embolic stroke. Stroke, 43, 2794–2799.
pubmed: 22910893
pmcid: 3740528
doi: 10.1161/STROKEAHA.112.660373
Ibrahim, A. S., Elmasry, K., Wan, M., Abdulmoneim, S., Still, A., Khan, F., et al. (2018). A controlled impact of optic nerve as a new model of traumatic optic neuropathy in mouse. Investigative Ophthalmology & Visual Science, 59, 5548–5557.
doi: 10.1167/iovs.18-24773
Ivanova, E., Alam, N. M., Prusky, G. T., & Sagdullaev, B. T. (2019). Blood-retina barrier failure and vision loss in neuron-specific degeneration. JCI Insight, 5(8), e126747.
doi: 10.1172/jci.insight.126747
Izzotti, A., Bagnis, A., & Sacca, S. C. (2006). The role of oxidative stress in glaucoma. Mutation Research, 612, 105–114.
pubmed: 16413223
doi: 10.1016/j.mrrev.2005.11.001
Ju, T. C., Chen, H. M., Chen, Y. C., Chang, C. P., Chang, C., & Chern, Y. (2014). AMPK-alpha1 functions downstream of oxidative stress to mediate neuronal atrophy in Huntington’s disease. Biochimica et Biophysica Acta, 1842, 1668–1680.
pubmed: 24946181
doi: 10.1016/j.bbadis.2014.06.012
Kaur, C., Foulds, W. S., & Ling, E. A. (2008). Hypoxia-ischemia and retinal ganglion cell damage. Clinical Ophthalmology, 2, 879–889.
pubmed: 19668442
pmcid: 2699791
doi: 10.2147/OPTH.S3361
Kaur, C., Rathnasamy, G., & Ling, E. A. (2013). Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina. Journal of Neuroimmune Pharmacology, 8, 66–78.
pubmed: 22367679
doi: 10.1007/s11481-012-9347-2
Khan, M. B., Hafez, S., Hoda, M. N., Baban, B., Wagner, J., Awad, M. E., et al. (2018). Chronic remote ischemic conditioning is cerebroprotective and induces vascular remodeling in a VCID model. Translational Stroke Research, 9, 51–63.
pubmed: 28755277
doi: 10.1007/s12975-017-0555-1
Kubota, S., Ozawa, Y., Kurihara, T., Sasaki, M., Yuki, K., Miyake, S., et al. (2011). Roles of AMP-activated protein kinase in diabetes-induced retinal inflammation. Investigative Ophthalmology & Visual Science, 52, 9142–9148.
doi: 10.1167/iovs.11-8041
Kumaran, A. M., Sundar, G., & Chye, L. T. (2015). Traumatic optic neuropathy: A review. Craniomaxillofacial Trauma Reconstruction, 8, 31–41.
pubmed: 25709751
doi: 10.1055/s-0034-1393734
Levin, L. A. (2004). Neuro-ophthalmologic diagnosis and therapy of central nervous system trauma. Ophthalmology Clinics of North America, 17, 455–464vii.
pubmed: 15337200
doi: 10.1016/j.ohc.2004.05.008
Li, J., Hu, X. S., Zhou, F. F., Li, S., Lin, Y. S., Qi, W. Q., et al. (2018). Limb remote ischemic postconditioning protects integrity of the blood-brain barrier after stroke. Neural Regeneration Research, 13, 1585–1593.
pubmed: 30127119
pmcid: 6126140
doi: 10.4103/1673-5374.237122
Li, S., Hu, X., Zhang, M., Zhou, F., Lin, N., Xia, Q., et al. (2015). Remote ischemic post-conditioning improves neurological function by AQP4 down-regulation in astrocytes. Behavioural Brain Research, 289, 1–8.
pubmed: 25907740
doi: 10.1016/j.bbr.2015.04.024
pmcid: 25907740
Li, S. Y., Yang, D., Yeung, C. M., Yu, W. Y., Chang, R. C., So, K. F., et al. (2011). Lycium barbarum polysaccharides reduce neuronal damage, blood-retinal barrier disruption and oxidative stress in retinal ischemia/reperfusion injury. PLoS ONE, 6, e16380.
pubmed: 21298100
pmcid: 3027646
doi: 10.1371/journal.pone.0016380
Liu, X., Sha, O., & Cho, E. Y. (2013). Remote ischemic postconditioning promotes the survival of retinal ganglion cells after optic nerve injury. Journal of Molecular Neuroscience, 51, 639–646.
pubmed: 23733254
doi: 10.1007/s12031-013-0036-2
pmcid: 23733254
Magharious, M. M., D’Onofrio, P. M., & Koeberle, P. D. (2011). Optic nerve transection: A model of adult neuron apoptosis in the central nervous system. Journal of Visualized Experiments, 51, 2241.
Mancini, S. J., & Salt, I. P. (2018). Investigating the role of AMPK in inflammation. Methods in Molecular Biology, 1732, 307–319.
pubmed: 29480484
doi: 10.1007/978-1-4939-7598-3_20
Meng, R., Asmaro, K., Meng, L., Liu, Y., Ma, C., Xi, C., et al. (2012). Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology, 79, 1853–1861.
pubmed: 23035060
doi: 10.1212/WNL.0b013e318271f76a
Murry, C. E., Jennings, R. B., & Reimer, K. A. (1986). Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation, 74, 1124–1136.
pubmed: 3769170
doi: 10.1161/01.CIR.74.5.1124
Oku, H., Kida, T., Horie, T., Taki, K., Mimura, M., Kojima, S., & Ikeda, T. (2019). Tau is involved in death of retinal ganglion cells of rats from optic nerve crush. Investigative Ophthalmology & Visual Science, 60, 2380–2387.
doi: 10.1167/iovs.19-26683
Olivier, S., Leclerc, J., Grenier, A., Foretz, M., Tamburini, J., & Viollet, B. (2019). AMPK Activation promotes tight junction assembly in intestinal epithelial Caco-2 Cells. International Journal of Molecular Sciences, 20, 5171.
pmcid: 6829419
doi: 10.3390/ijms20205171
pubmed: 6829419
Park, S. Y., Choi, M. H., Li, M., Li, K., Park, G., & Choi, Y. W. (2018). AMPK/Nrf2 signaling is involved in the anti-neuroinflammatory action of Petatewalide B from Petasites japonicus against lipopolysaccharides in microglia. Immunopharmacology and Immunotoxicology, 40, 232–241.
pubmed: 29433360
doi: 10.1080/08923973.2018.1434791
Peixoto, C. A., Oliveira, W. H., Araujo, S., & Nunes, A. K. S. (2017). AMPK activation: Role in the signaling pathways of neuroinflammation and neurodegeneration. Experimental Neurology, 298, 31–41.
pubmed: 28844606
doi: 10.1016/j.expneurol.2017.08.013
Sanes, J. R., & Masland, R. H. (2015). The types of retinal ganglion cells: Current status and implications for neuronal classification. Annual Review of Neuroscience, 38, 221–246.
pubmed: 25897874
doi: 10.1146/annurev-neuro-071714-034120
Siqueira Mietto, B., Kroner, A., Girolami, E. I., Santos-Nogueira, E., Zhang, J., & David, S. (2015). Role of IL-10 in resolution of inflammation and functional recovery after peripheral nerve injury. Journal of Neuroscience, 35, 16431–16442.
pubmed: 26674868
doi: 10.1523/JNEUROSCI.2119-15.2015
Steinsapir, K. D., & Goldberg, R. A. (2011). Traumatic optic neuropathy: An evolving understanding. American Journal of Ophthalmology, 151(928–933), e922.
Tang, Z., Zhang, S., Lee, C., Kumar, A., Arjunan, P., Li, Y., et al. (2011). An optic nerve crush injury murine model to study retinal ganglion cell survival. Journal of Visualized Experiments, 50, 2685.
Tao, W., Dvoriantchikova, G., Tse, B. C., Pappas, S., Chou, T. H., Tapia, M., et al. (2017). A novel mouse model of traumatic optic neuropathy using external ultrasound energy to achieve focal, indirect optic nerve injury. Scientific Reports, 7, 11779.
pubmed: 28924145
pmcid: 5603527
doi: 10.1038/s41598-017-12225-6
Tezel, G., Yang, X., Yang, J., & Wax, M. B. (2004). Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Research, 996, 202–212.
pubmed: 14697498
doi: 10.1016/j.brainres.2003.10.029
Tong, N., Zhang, Z., Zhang, W., Qiu, Y., Gong, Y., Yin, L., et al. (2013). Diosmin alleviates retinal edema by protecting the blood-retinal barrier and reducing retinal vascular permeability during ischemia/reperfusion injury. PLoS ONE, 8, e61794.
pubmed: 23637907
pmcid: 3634841
doi: 10.1371/journal.pone.0061794
Tse, B. C., Dvoriantchikova, G., Tao, W., Gallo, R. A., Lee, J. Y., Pappas, S., et al. (2018). Tumor necrosis factor inhibition in the acute management of traumatic optic neuropathy. Investigative Ophthalmology & Visual Science, 59, 2905–2912.
doi: 10.1167/iovs.18-24431
Tulsawani, R., Kelly, L. S., Fatma, N., Chhunchha, B., Kubo, E., Kumar, A., & Singh, D. P. (2010). Neuroprotective effect of peroxiredoxin 6 against hypoxia-induced retinal ganglion cell damage. BMC Neuroscience, 11, 125.
pubmed: 20923568
pmcid: 2964733
doi: 10.1186/1471-2202-11-125
Vaibhav, K., Braun, M., Khan, M. B., Fatima, S., Saad, N., Shankar, A., et al. (2018). Remote ischemic post-conditioning promotes hematoma resolution via AMPK-dependent immune regulation. Journal of Experimental Medicine, 215, 2636–2654.
doi: 10.1084/jem.20171905
Wilson, C. A., Berkowitz, B. A., Funatsu, H., Metrikin, D. C., Harrison, D. W., Lam, M. K., & Sonkin, P. L. (1995). Blood-retinal barrier breakdown following experimental retinal ischemia and reperfusion. Experimental Eye Research, 61, 547–557.
pubmed: 8654497
doi: 10.1016/S0014-4835(05)80048-X
Xu, L., Kong, L., Wang, J., & Ash, J. D. (2018). Stimulation of AMPK prevents degeneration of photoreceptors and the retinal pigment epithelium. Proceedings of the National Academy of Sciences of the United States of America, 115, 10475–10480.
pubmed: 30249643
pmcid: 6187182
doi: 10.1073/pnas.1802724115
Yang, W. R., Liao, T. T., Bao, Z. Q., Zhou, C. Q., Luo, H. Y., Lu, C., et al. (2018). Role of AMPK in the expression of tight junction proteins in heat-treated porcine Sertoli cells. Theriogenology, 121, 42–52.
pubmed: 30125827
doi: 10.1016/j.theriogenology.2018.08.005
Yu-Wai-Man, P. (2015). Traumatic optic neuropathy-clinical features and management issues. Taiwan Journal of Ophthalmology, 5, 3–8.
pubmed: 26052483
pmcid: 4457437
doi: 10.1016/j.tjo.2015.01.003
Yu-Wai-Man, P., & Griffiths, P. G. (2011). Steroids for traumatic optic neuropathy. Cochrane Database of Systematic Reviews, 1, CD006032.
Zhang, X., Jizhang, Y., Xu, X., Kwiecien, T. D., Li, N., Zhang, Y., et al. (2014). Protective effects of remote ischemic conditioning against ischemia/reperfusion-induced retinal injury in rats. Visual Neuroscience, 31, 245–252.
pubmed: 24735565
doi: 10.1017/S0952523814000121
Zhao, Q., Ji, M., & Wang, X. (2018). IL-10 inhibits retinal pigment epithelium cell proliferation and migration through regulation of VEGF in rhegmatogenous retinal detachment. Molecular Medicine Reports, 17, 7301–7306.
pubmed: 29568872
Zhao, Y., Hu, X., Liu, Y., Dong, S., Wen, Z., He, W., et al. (2017). ROS signaling under metabolic stress: Cross-talk between AMPK and AKT pathway. Molecular Cancer, 16, 79.
pubmed: 28407774
pmcid: 5390360
doi: 10.1186/s12943-017-0648-1
Zhu, Y. P., Brown, J. R., Sag, D., Zhang, L., & Suttles, J. (2015). Adenosine 5’-monophosphate-activated protein kinase regulates IL-10-mediated anti-inflammatory signaling pathways in macrophages. The Journal of Immunology, 194, 584–594.
pubmed: 25512602
doi: 10.4049/jimmunol.1401024