Protective effects of remote ischemic conditioning against ischemia/reperfusion-induced retinal injury in rats

Visual Neuroscience

Volumn 31, Issue 3, 2014, Pages 245-252

  Zhang, Xuxiang ^a   Jizhang, Yunneng ^a,b   Xu, Xiaoying ^a   Kwiecien, Timothy D ^c   Li, Ning ^a   Zhang, Ying ^a   Ji, Xunming ^a   Ren, Changhong ^a   Ding, Yuchuan ^c  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b Brownell Talbot School   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glial fibrillary acidic protein; Heme oxygenase 1; Nuclear factor erythroid 2 related factor 2; Remote ischemic conditioning; Retinal injury

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HEME OXYGENASE 1; TRANSCRIPTION FACTOR NRF2; NFE2L2 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; ISCHEMIC POSTCONDITIONING; LIMB REMOTE ISCHEMIC CONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; RETINA GANGLION CELL; RETINA INJURY; RETINA ISCHEMIA; UPREGULATION; ADULT; ANIMAL CELL; CELL COUNT; HISTOPATHOLOGY; ISCHEMIC PRECONDITIONING; TOURNIQUET; ANIMAL; CEREBRAL ARTERY DISEASE; COMPLICATION; DISEASE MODEL; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; PROCEDURES; RETINAL DISEASES; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HEME OXYGENASE-1; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIC PRECONDITIONING; MALE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RETINAL DISEASES; TIME FACTORS;

EID: 84901331391     PISSN: 09525238     EISSN: 14698714     Source Type: Journal    
DOI: 10.1017/S0952523814000121     Document Type: Article

References (37)

1. Arai-Gaun, S., Katai, N., Kikuchi, T., Kurokawa, T., Ohta, K. & Yoshimura, N. (2004). Heme oxygenase-1 induced in muller cells plays a protective role in retinal ischemia-reperfusion injury in rats. Investigative Ophthalmology & Visual Science 45, 4226-4232
2. Block, F., Grommes, C., Kosinski, C., Schmidt, W. & Schwarz, M. (1997). Retinal ischemia induced by the intraluminal suture method in rats. Neuroscience Letters 232, 45-48
3. Botker, H.E., Kharbanda, R., Schmidt, M.R., Bottcher, M., Kaltoft, A.K., Terkelsen, C.J., Munk, K., Andersen, N.H., Hansen, T.M., Trautner, S., Lassen, J.F., Christiansen, E.H., Krusell, L.R., Kristensen, S.D., Thuesen, L., Nielsen, S.S., Rehling, M., Sorensen, H.T., Redington, A.N. & Nielsen, T.T. (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. Lancet 375, 727-734
4. Dreixler, J.C., Bratton, A., Du, E., Shaikh, A.R., Savoie, B., Alexander, M., Marcet, M.M & Roth, S. (2011 a). Mitogenactivated protein kinase phosphatase-1 (MKP-1) in retinal ischemic preconditioning. E xperimental Eye Research 93, 340-349
5. Dreixler, J.C., Sampat, A., Shaikh, A.R., Alexander, M., Marcet, M.M & Roth, S. (2011 b). Protein kinase B (Akt) and mitogen-Activated protein kinase p38alpha in retinal ischemic post-conditioning. Journal of Molecular Neuroscience 45, 309-320
6. Eng, L.F., Ghirnikar, R.S. & Lee, Y.L. (2000). Glial fi brillary acidic protein: GFAP-Thirty-one years (1969-2000). Neurochemical Research 25, 1439-1451
7. Fernandez, D.C., Bordone, M.P., Chianelli, M.S. & Rosenstein, R.E. (2009 a). Retinal neuroprotection against ischemia-reperfusion damage induced by postconditioning. Investigative Ophthalmology & Visual Science 50, 3922-3930
8. Fernandez, D.C., Chianelli, M.S. & Rosenstein, R.E. (2009 b). Involvement of glutamate in retinal protection against ischemia/reperfusion damage induced by post-conditioning. Journal of Neurochemistry 111, 488-498
9. Flammer, J., Orgul, S., Costa, V.P., Orzalesi, N., Krieglstein, G.K., Serra, L.M., Renard, J.P. & Stefansson, E. (2002). The impact of ocular blood fl ow in glaucoma. Progress in Retinal and Eye Research 21, 359-393
10. Hausenloy, D.J. & Yellon, D.M. (2008). Remote ischaemic preconditioning: Underlying mechanisms and clinical application. Cardiovascular Research 79, 377-386
11. Hausenloy, D.J. & Yellon, D.M. (2011). The therapeutic potential of ischemic conditioning: An update. Nature Reviews Cardiology 8, 619-629
12. He, M., Pan, H., Chang, R.C., So, K.F., Brecha, N.C. & Pu, M. (2014). Activation of the Nrf2/HO-1 antioxidant pathway contributes to the protective effects of Lycium barbarum polysaccharides in the rodent retina after ischemia-reperfusion-induced damage. PLoS One 9, e84800
13. Hoda, M.N., Siddiqui, S., Herberg, S., Periyasamy-Thandavan, S., Bhatia, K., Hafez, S.S., Johnson, M.H., Hill, W.D., Ergul, A., Fagan, S.C. & Hess, D.C. (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
14. Jadhav, A.P., Roesch, K. & Cepko, C.L. (2009). Development and neurogenic potential of Muller glial cells in the vertebrate retina. Progress in Retinal and Eye Research 28, 249-262
15. Lai, I.R., Chang, K.J., Chen, C.F. & Tsai, H.W. (2006). Transient limb ischemia induces remote preconditioning in liver among rats: The protective role of heme oxygenase-1. Transplantation 81, 1311-1317
16. Lee, J.M., Calkins, M.J., Chan, K., Kan, Y.W. & Johnson, J.A. (2003). Identifi cation of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. The Journal of Biological Chemistry 278, 12029-12038. (Pubitemid 36800179
17. Li, S.Y., Fu, Z.J. & Lo, A.C. (2012). Hypoxia-induced oxidative stress in ischemic retinopathy. Oxidative Medicine and Cellular Longevity 2012, 426769
18. Meng, R., Asmaro, K., Meng, L., Liu, Y., Ma, C., Xi, C., Li, G., Ren, C., Luo, Y., Ling, F., Jia, J., Hua, Y., Wang, X., Ding, Y., Lo, E.H. & Ji, X. (2012). Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79, 1853-1861
19. Moi, P., Chan, K., Asunis, I., Cao, A. & Kan, Y.W. (1994). Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proceedings of the National Academy of Sciences of the United States of America 91, 9926-9930
20. Obolensky, A., Berenshtein, E., Konijn, A.M., Banin, E. & Chevion, M. (2008). Ischemic preconditioning of the rat retina: Protective role of ferritin. Free Radical Biology & Medicine 44, 1286-1294
21. Osborne, N.N., Block, F. & Sontag, K.H. (1991). Reduction of ocular blood fl ow results in glial fi brillary acidic protein (GFAP) expression in rat retinal Muller cells. Visual Neuroscience 7, 637-639
22. Osborne, N.N., Casson, R.J., Wood, J.P., Chidlow, G., Graham, M. & Melena, J. (2004). Retinal ischemia: Mechanisms of damage and potential therapeutic strategies. Progress in Retinal and Eye Research 23, 91-147
23. Owuor, E.D. & Kong, A.N. (2002). Antioxidants and oxidants regulated signal transduction pathways. Biochemical Pharmacology 64, 765-770
24. Ren, C., Gao, M., Dornbos, D. 3rd, Ding, Y., Zeng, X., Luo, Y. & Ji, X. (2012). Remote ischemic post-conditioning reduced brain damage in experimental ischemia/reperfusion injury. Neurological Research 33, 514-519
25. Satoh, T., Okamoto, S.I., Cui, J., Watanabe, Y., Furuta, K., Suzuki, M., Tohyama, K. & Lipton, S.A. (2006). Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophilic] phase II inducers. Proceedings of the National Academy of Sciences of the United States of America 103, 768-773
26. Saxena, P., Newman, M.A., Shehatha, J.S., Redington, A.N. & Konstantinov, I.E. (2010). Remote ischemic conditioning: Evolution of the concept, mechanisms, and clinical application. Journal of Cardiac Surgery 25, 127-134
27. Shah, Z.A., Li, R., Thimmulappa, R.K., Kensler, T.W., Yamamoto, M., Biswal, S. & Dore, S. (2007). Role of reactive oxygen species in modulation of Nrf2 following ischemic reperfusion injury. Neuroscience 147, 53-59
28. Shelton, P. & Jaiswal, A.K. (2013). The transcription factor NF-E2-related factor 2 (Nrf2): A protooncogene?. FASEB Journal 27, 414-423
29. Shokeir, A.A., Hussein, A.M., Barakat, N., Abdelaziz, A., Elgarba, M. & Awadalla, A. (2014). Activation of nuclear factor erythroid 2-related factor 2 (Nrf2) and Nrf-2-dependent genes by ischaemic pre-conditioning and post-conditioning: New adaptive endogenous protective responses against renal ischaemia/reperfusion injury. Acta Physiologica (Oxford). 210, 342-353
30. Veighey, K. & Macallister, R.J. (2012). Clinical applications of remote ischemic preconditioning. Cardiology Research and Practice 2012, 620681
31. Verma, D (1993). Pathogenesis of diabetic retinopathy-The missing link?. Medical Hypotheses 41, 205-210
32. Wei, M., Xin, P., Li, S., Tao, J., Li, Y., Li, J., Liu, M., Zhu, W. & Redington, A.N. (2011). Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circulation Research 108, 1220-1225
33. Zhang, C., Rosenbaum, D.M., Shaikh, A.R., Li, Q., Rosenbaum, P.S., Pelham, D.J. & Roth, S. (2002). Ischemic preconditioning attenuates apoptotic cell death in the rat retina. Investigative Ophthalmology & Visual Science 43, 3059-3066
34. Zhao, H. (2009). Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. Journal of Cerebral Blood Flow and Metabolism 29, 873-885
35. Zhao, J., Kobori, N., Aronowski, J. & Dash, P.K. (2006). Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neuroscience Letters 393, 108-112
36. Zhao, Z.Q. & Vinten-Johansen, J. (2006). Postconditioning: Reduction of reperfusion-induced injury. Cardiovascular Research 70, 200-211
37. Zhu, Y., Zhang, Y., Ojwang, B.A., Brantley, M.A. Jr. & Gidday, J.M. (2007). Long-Term tolerance to retinal ischemia by repetitive hypoxic preconditioning: Role of HIF-1alpha and heme oxygenase-1. Investigative Ophthalmology & Visual Science 48, 1735-1743