Chitosan oligosaccharides prevented retinal ischemia and reperfusion injury via reduced oxidative stress and inflammation in rats

Experimental Eye Research

Volumn 130, Issue , 2015, Pages 38-50

  Fang, I Mo ^a,b   Yang, Chung May ^b   Yang, Chang Hao ^b  

^a TAIPEI CITY HOSPITAL   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Chitosan oligosaccharides; COS; ERG; I R; Ischemia reperfusion injury; Mitogen activated protein kinases (MAPK); NF B; Oxidative damage; RGCs; ROS; TUNEL

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 8 HYDROXYDEOXYGUANOSINE; AGENTS ACTING ON THE EYE; BETA ACTIN; CHITOSAN; CHITOSAN OLIGOSACCHARIDE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; OLIGOSACCHARIDE; PHOSPHATE BUFFERED SALINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CCL2 PROTEIN, RAT; CHELATING AGENT; MESSENGER RNA; NOS2 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; B WAVE; BINDING AFFINITY; CELL DENSITY; CELL SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG MEGADOSE; ELECTRORETINOGRAM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; EYE PROTECTION; GEL MOBILITY SHIFT ASSAY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; LOW DRUG DOSE; MORPHOLOGY; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; RETINA; RETINA GANGLION CELL; RETINA ISCHEMIA; RETINAL THICKNESS; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; ELECTRORETINOGRAPHY; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; RETINAL DISEASES; SPRAGUE DAWLEY RAT; TUNEL ASSAY;

ANIMALS; BLOTTING, WESTERN; CHELATING AGENTS; CHEMOKINE CCL2; CHITOSAN; ELECTRORETINOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; I-KAPPA B PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-1BETA; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RETINAL DISEASES; RETINAL GANGLION CELLS; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84914165761     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.12.001     Document Type: Article

References (47)

1. Aggarwal B.B. Apoptosis and nuclear factor-kappa B: a tale of association and dissociation. Biochem. Pharmacol. 2000, 60:1033-1039.
2. Barone F.C., Arvin B., White R.F., Miller A., Webb C.L., Willette R.N., Lysko P.G., Feuerstein G.Z. Tumor necrosis factor-alpha. A mediator of focal ischemic brain injury. Stroke 1997, 28:1233-1244.
3. Bates S., Vousden K.H. Mechanisms of p53-mediated apoptosis. Cell. Mol. Life Sci. 1999, 55:28-37.
4. Biermann J., Lagreze W.A., Dimitriu C., Stoykow C., Goebel U. Preconditioning with inhalative carbon monoxide protects rat retinal ganglion cells from ischemia/reperfusion injury. Investig. Ophthalmol. Vis. Sci. 2010, 51:3784-3791.
5. Chen J., Fujii K., Zhang L., Roberts T., Fu H. Raf-1 promotes cell survival by antagonizing apoptosis signal-regulating kinase 1 through a MEK-ERK independent mechanism. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7783-7788.
6. Chen Q., Liu S.Q., Du Y.M., Peng H., Sun L.P. Carboxymethyl -chitosan protects rabbit chondrocytes from interleukin-1beta-induced apoptosis. Eur. J. Pharmacol. 2006, 541:1-8.
7. Dreixler J.C., Barone F.C., Shaikh A.R., Du E., Roth S. Mitogen -activated protein kinase p38α and retinal ischemic preconditioning. Exp. Eye Res. 2009, 89:782-790.
8. Dvoriantchikova G., Barakat D., Brambilla R., Agudelo C., Hernandez E., Bethea J.R., Shestopalov V.I., Ivanov D. Inactivation of astroglial NF-kappa B promotes survival of retinal neurons following ischemic injury. Eur. J. Neurosci. 2009, 30:175-185.
9. Dvoriantchikova G., Agudelo C., Hernandez E., Shestopalov V.I., Ivanov D. Phosphatidylserine-containing liposomes promote maximal survival of retinal neurons after ischemic injury. J.Cereb. Blood Flow Metab. 2009, 29:1755-1759.
10. Fontaine V., Mohand-Said S., Hanoteau N., Fuchs C., Pfizenmaier K., Eisel U. Neurodegenerative and neuroprotective effects of tumor Necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J.Neurosci. 2002, 22:RC216.
11. Gustavsson C., Agardh C.D., Hagert P., Agardh E. Inflammatory markers in nondiabetic and diabetic rat retinas exposed to ischemia followed by reperfusion. Retina 2008, 28:645-652.
12. Hangai M., Yoshimura N., Honda Y. Increased cytokine gene expression in rat retina following transient ischemia. Ophthalmic Res. 1996, 28:248-254.
13. Ishizuka F., Shimazawa M., Umigai N., Ogishima H., Nakamura S., Tsuruma K., Hara H. Crocetin, a carotenoid derivative, inhibits retinal ischemic damage in mice. Eur. J. Pharmacol. 2013, 703:1-10.
14. Je J.Y., Park P.J., Kim S.K. Free radical scavenging properties of hetero- chitooligosaccharides using an ESR spectroscopy. Food Chem. Toxicol. 2004, 42:381-387.
15. Jiang S.Y., Zou Y.Y., Wang J.T. p38 mitogen-activated protein kinase-induced nuclear factor kappa-light-chain-enhancer of activated B cell activity is required for neuroprotection in retinal ischemia/reperfusion injury. Mol. Vis. 2012, 18:2096-2106.
16. Jo N., Wu G.S., Rao N.A. Up-regulation of chemokine expression in the retinal vasculature in ischemia-reperfusion injury. Investig. Ophthalmol. Vis. Sci. 2003, 44:4054-4060.
17. Joodi G., Ansari N., Khodagholi F. Chitooligosaccharide-mediated neuroprotection is associated with modulation of Hsps expression and reduction of MAPK phosphorylation. Int. J. Biol. Macromol. 2011, 48:726-735.
18. Ju W.K., Lindsey J.D., Angert M., Patel A., Weinreb R.N. Glutamate receptor activation triggers OPA1 release and induces apoptotic cell death in ischemic rat retina. Mol. Vis. 2008, 14:2629-2638.
19. Khodagholi F., Eftekharzadeh B., Maghsoudi N., Rezaei P.F. Chitosan prevents oxidative stress-induced amyloid beta formation and cytotoxicity in NT2 neurons: involvement of transcription factors Nrf2 and NF-kappa B. Mol. Cell. Biochem. 2010, 337:39-51.
20. Lam T.T., Abler A.S., Tao M.O.M. Apoptosis and caspase after ischemia-reperfusion injury in rat retina. Investig. Ophthalmol. Vis. Sci. 1999, 40:967-975.
21. Laskowski I., Pratschke J., Wilhelm M.J., Gasser M., Tilney N.L. Molecular and cellular events associated with ischemia/reperfusion injury. Ann. Transpl. 2000, 5:29-35.
22. Levine L.A. Models of neural injury. J.Glaucoma 2001, 10:S19-S21.
23. Liang Z.Q., Li Y.L., Zhao X.L., Han R., Wang X.X., Wang Y., Chase T.N., Bennett M.C., Qin Z.H. NF-kappaB contributes to 6-hydroxydopamine -induced apoptosis of nigral dopaminergic neurons through p53. Brain Res. 2007, 1145:190-203.
24. Osborne N.N., Casson R.J., Wood J.P., Chidlow G., Graham M., Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog. Retin. Eye Res. 2004, 23:91-147.
25. Pae H.O., Seo W.G., Kim N.Y., Oh G.S., Kim G.E., Kim Y.H., Kwak H.J., Yun Y.G., Jun C.D., Chung H.T. Induction of granulocytic differentiation in acute promyelocytic leukemia cells (HL-60) by water-soluble chitosan oligomer. Leuk. Res. 2001, 25:339-346.
26. Pangestuti R., Kim S.K. Neuroprotective properties of chitosan and its derivatives. Mar. Drugs 2010, 8:2117-2128.
27. Qi Y., Chen L., Zhang L., Liu W.B., Chen X.Y., Yang X.G. Crocin prevents retinal ischaemia/reperfusion injury-induced apoptosis in retinal ganglion cells through the PI3K/AKT signalling pathway. Exp. Eye Res. 2013, 107:44-45.
28. Qin Z.H., Chen R.W., Wang Y., Nakai M., Chuang D.M., Chase T.N. Nuclear factor kappaB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J.Neurosci. 1999, 19:4023-4033.
29. Qin C., Du Y., Xiao L., Li Z., Gao X. Enzymic preparation of water-soluble chitosan and their antitumor activity. Int. J. Biol. Macromol. 2002, 31:1111-1117.
30. Roth S., Shaikh A.R., Hennelly M.M., Li Q., Bindokas V., Graham C.E. Mitogen-activated protein kinases and retinal ischemia. Investig. Ophthalmol. Vis. Sci. 2003, 44:5383-5395.
31. Ryan K.M., Phillips A.C., Vousden K.H. Regulation and function of the p53 tumor suppressor protein. Curr. Opin. Cell. Biol. 2001, 13:33-337.
32. Samdani A.F., Dawson T.M., Dawson V.L. Nitric oxide synthase in models of focal ischemia. Sroke 1997, 28:1283-1288.
33. Schreck R., Albermann K., Baeuerle P.A. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells. Free Radic. Res. Commun. 1992, 17:221-237.
34. Stefansson E., Machemer R., de Juan E., McCuen B.W., Peterson J. Retinal oxygenation and laser treatment in patients with diabetic retinopathy. Am. J. Ophthalmol. 1992, 113:36-38.
35. Sun M.H., Pang J.H., Chen S.L., Han W.H., Ho T.C., Chen K.J., Kao L.Y., Lin K.K., Tsao Y.P. Retinal protection from acute glaucoma-induced ischemia-reperfusion injury through pharmacologic induction of heme oxygenase-1. Investig. Ophthalmol. Vis. Sci. 2010, 51:4798-4808.
36. Szabo M.E., Droy-Lefaix M.T., Doly M., Carré C., Braquet P. Ischemia and reperfusion-induced histologic changes in the rat retina. Demonstration of a free radical-mediated mechanism. Investig. Ophthalmol. Vis. Sci. 1991, 32:1471-1478.
37. Tang G., Minemoto Y., Dibling B., Purcell N.H., Li Z., Karin M., Lin A. Inhibition of JNK activation through NF-kappaB target genes. Nature 2001, 414:313-317.
38. Tezel G., Wax M.B. Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J.Neurosci. 2000, 20:8693-8700. http://www.iovs.org/external-ref?access_num=10.1038/35104568%26link_type=DOI.
39. Tian D., Litvak V., Lev S. Cerebral ischemia and seizures induce tyrosine phosphorylation of PYK2 in neurons and microglial cells. J.Neurosci. 2000, 20:6478-6487.
40. Tso M.O., Jampol L.M. Pathophysiology of hypertensive retinopathy. Ophthalmology 1982, 89:1132-1145.
41. Wei P., Ma P., Xu Q.S., Bai Q.H., Gu J.G., Xi H., Du Y.G., Yu C. Chitosan oligosaccharides suppress production of nitric oxide in lipopoly -saccharide-induced N9 murine microglial cells invitro. Glycoconj. J. 2012, 29:285-295.
42. Wu W.C., Lai C.C., Chen S.L., Sun M.H., Xiao X., Chen T.L., Tsai R.J., Kuo S.W., Tsao Y.P. GDNF gene therapy attenuates retinal ischemic injuries in rats. Mol. Vis. 2004, 10:93-102.
43. Xie W., Xu P., Liu Q. Antioxidant activity of water-soluble chitosan derivatives. Bioorg. Med. Chem. Lett. 2001, 11:1699-1701.
44. Yokota H., Narayanan S.P., Zhang W., Liu H., Rojas M., Xu Z., Lemtalsi T., Nagaoka T., Yoshida A., Brooks S.E., Caldwell R.W., Caldwell R.B. Neuroprotection from retinal ischemia/reperfusion injury by NOX2 NADPH oxidase deletion. Investig. Ophthalmol. Vis. Sci. 2011, 52:8123-8131.
45. Yoneda S., Tanihara H., Kido N., Honda Y., Goto W., Hara H., Miyawaki N. Interleukin-1β mediates ischemic injury in the rat retina. Exp. Eye Res. 2001, 73:661-667.
46. Zheng L., Gong B., Hatala D.A., Kern T.S. Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes. Investig. Ophthalmol. Vis. Sci. 2007, 48:361-367.
47. Zhang X.Y., Xiao Y.Q., Zhang Y., Ye W. Protective effect of pioglitazone on retinal ischemia/reperfusion injury in rats. Investig. Ophthalmol. Vis. Sci. 2013, 54:3912-3921.