Dynamic, invivo, real-time detection of retinal oxidative status in a model of elevated intraocular pressure using a novel, reversibly responsive, profluorescent nitroxide probe

Experimental Eye Research

Volumn 129, Issue , 2014, Pages 48-56

  Rayner, Cassie L ^a   Gole, Glen A ^b   Bottle, Steven E ^c   Barnett, Nigel L ^a,c,d  

^a QUEENSLAND EYE INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Fluorescent probe; Ischemia; Nitroxide; Oxidative stress; Reactive oxygen species; Reperfusion; Retina

Indexed keywords

ANTIOXIDANT; NITROXIDE; REACTIVE OXYGEN METABOLITE; XANTHOPHYLL; FLUORESCENT DYE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAPHY; FEMALE; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTRAOCULAR PRESSURE; NONHUMAN; OXIDATIVE STRESS; RAT; REPERFUSION; RETINA INJURY; RETINA ISCHEMIA; ANIMAL; CONVALESCENCE; DIAGNOSTIC USE; DISEASE MODEL; GLAUCOMA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; SPRAGUE DAWLEY RAT;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FEMALE; FLUORESCENT DYES; GLAUCOMA; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECOVERY OF FUNCTION; RETINA;

EID: 84910086581     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.10.013     Document Type: Article

References (91)

1. Abramov A.Y., Scorziello A., Duchen M.R. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J.Neurosci. 2007, 27:1129-1138.
2. Ahn H.-Y., Fairfull-Smith K.E., Morrow B.J., Lussini V., Kim B., Bondar M.V., Bottle S.E., Belfield K.D. Two-photon fluorescence microscopy imaging of cellular oxidative stress using profluorescent nitroxides. J.Am. Chem. Soc. 2012, 134:4721-4730.
3. Aliev G., Priyadarshini M., Reddy V., Grieg N., Kaminsky Y., Cacabelos R., Ashraf G., Jabir N., Kamal M., Nikolenko V. Oxidative stress mediated mitochondrial and vascular lesions as markers in the pathogenesis of Alzheimer disease. Curr. Med. Chem. 2013, 21:2208-2217.
4. Almasieh M., Wilson A.M., Morquette B., Cueva Vargas J.L., Di Polo A. The molecular basis of retinal ganglion cell death in glaucoma. Prog. Retin. Eye Res. 2012, 31:152-181.
5. Alves-Rodrigues A., Shao A. The science behind lutein. Toxicol. Lett. 2004, 150:57-83.
6. Arend O., Plange N., Sponsel W.E., Remky A. Pathogenetic aspects of the glaucomatous optic neuropathy: fluorescein angiographic findings in patients with primary open angle glaucoma. Brain Res. Bull. 2004, 62:517-524.
7. Aydemir O., Naziroğlu M., Çelebi S., Yilmaz T., Kükner A.Ş. Antioxidant effects of alpha-, gamma-and succinate-tocopherols in guinea pig retina during ischemia-reperfusion injury. Pathophysiology 2004, 11:167-171.
8. Azad M.B., Chen Y., Gibson S.B. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid. Redox Signal. 2009, 11:777-790.
9. Barnett N.L., Gole G.A., Rayner C.L., Chong K.L., Bottle S.E. Evaluation of a novel fluorescent probe for the assessment of retinal oxidative status. Clin. Exp. Ophthalmol 2013, 41. 126-126.
10. Barnham K.J., Masters C.L., Bush A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 2004, 3:205-214.
11. Bazan N.G. The metabolism of omega-3 polyunsaturated fatty acids in the eye: the possible role of docosahexaenoic acid and docosanoids in retinal physiology and ocular pathology. Prog. Clin. Biol. Res. 1988, 312:95-112.
12. Belkin S., Mehlhorn R.J., Hideg K., Hankovsky O., Packer L. Reduction and destruction rates of nitroxide spin probes. Arch. Biochem. Biophys. 1987, 256:232-243.
13. Block F., Schwarz M. Effects of antioxidants on ischemic retinal dysfunction. Exp. Eye Res. 1997, 64:559-564.
14. Blough N.V., Simpson D.J. Chemically mediated fluorescence yield switching in nitroxide-fluorophore adducts: optical sensors of radical/redox reactions. J.Am. Chem. Soc. 1988, 110:1915-1917.
15. Bush R.A., Sieving P.A. Inner retinal contributions to the primate photopic fast flicker electroretinogram. J.Opt. Soc. Am. A 1996, 13:557-565.
16. Celebi S., Dilsiz N., Yilmaz T., Kükner A.S. Effects of melatonin, vitamin E and octreotide on lipid peroxidation during ischemia-reperfusion in the guinea pig retina. Eur. J. Ophthalmol. 2001, 12:77-83.
17. Chasan-Taber L., Willett W.C., Seddon J.M., Stampfer M.J., Rosner B., Colditz G.A., Speizer F.E., Hankinson S.E. Aprospective study of carotenoid and vitamin A intakes and risk of cataract extraction in US women. Am. J. Clin. Nutr. 1999, 70:509-516.
18. Chen Y., McMillan-Ward E., Kong J., Israels S.J., Gibson S.B. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J.Cell Sci. 2007, 120:4155-4166.
19. Chidlow G., Schmidt K.-G., Wood J., Melena J., Osborne N. α-lipoic acid protects the retina against ischemia-reperfusion. Neuropharmacology 2002, 43:1015-1025.
20. Cho K.J., Kim J.H., Park H.-Y.L., Park C.K. Glial cell response and iNOS expression in the optic nerve head and retina of the rat following acute high IOP ischemia-reperfusion. Brain Res. 2011, 1403:67-77.
21. Chrysostomou V., Rezania F., Trounce I.A., Crowston J.G. Oxidative stress and mitochondrial dysfunction in glaucoma. Curr. Opin. Pharmacol. 2013, 13:12-15.
22. Chucair A.J., Rotstein N.P., SanGiovanni J.P., During A., Chew E.Y., Politi L.E. Lutein and zeaxanthin protect photoreceptors from apoptosis induced by oxidative stress: relation with docosahexaenoic acid. Investig. Ophthalmol. Vis. Sci. 2007, 48:5168-5177.
23. Chung H.S., Harris A., Evans D.W., Kagemann L., Garzozi H.J., Martin B. Vascular aspects in the pathophysiology of glaucomatous optic neuropathy. Surv. Ophthalmol. 1999, 43:S43-S50.
24. Dilsiz N., Sahaboglu A., Yildiz M.Z., Reichenbach A. Protective effects of various antioxidants during ischemia-reperfusion in the rat retina. Graefe's Arch. Clin. Exp. Ophthalmol. 2006, 244:627-633.
25. Dirani M., Crowston J.G., Taylor P.S., Moore P.T., Rogers S., Pezzullo M.L., Keeffe J.E., Taylor H.R. Economic impact of primary open-angle glaucoma in Australia. Clin. Exp. Ophthalmol. 2011, 39:623-632.
26. Fernandez-Suarez M., Ting A.Y. Fluorescent probes for super-resolution imaging in living cells. Nat. Rev. Mol. Cell Biol. 2008, 9:929-943.
27. Green S.A., Simpson D.J., Zhou G., Ho P.S., Blough N.V. Intramolecular quenching of excited singlet states by stable nitroxyl radicals. J.Am. Chem. Soc. 1990, 112:7337-7346.
28. Hall J.K., Andrews A.P., Walker R., Piltz-Seymour J.R. Association of retinal vessel caliber and visual field defects in glaucoma. Am. J. Ophthalmol. 2001, 132:855-859.
29. Halliwell B., Whiteman M. Measuring reactive species and oxidative damage invivo and in cell culture: how should you do it and what do the results mean?. Br. J. Pharmacol. 2004, 142:231-255.
30. Hamanaka R.B., Chandel N.S. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem. Sci. 2010, 35:505-513.
31. Hess M.L., Manson N.H. Molecular oxygen: friend and foe: the role of the oxygen free radical system in the calcium paradox, the oxygen paradox and ischemia/reperfusion injury. J.Mol. Cell. Cardiol. 1984, 16:969-985.
32. Hirosawa S., Arai S., Takeoka S. ATEMPO-conjugated fluorescent probe for monitoring mitochondrial redox reactions. Chem. Commun. 2012, 48:4845-4847.
33. Holcombe D.J., Lengefeld N., Gole G.A., Barnett N.L. The effects of acute intraocular pressure elevation on rat retinal glutamate transport. Acta Ophthalmol. 2008, 86:408-414.
34. Hood D.C., Birch D.G. b wave of the scotopic (rod) electroretinogram as a measure of the activity of human on-bipolar cells. J.Opt. Soc. Am. A 1996, 13:623-633.
35. Hughes W.F. Quantitation of ischemic damage in the rat retina. Exp. Eye Res. 1991, 53:573-582.
36. Itagaki S., Ogura W., Sato Y., Noda T., Hirano T., Mizuno S., Iseki K. Characterization of the disposition of lutein after iv administration to rats. Biol. Pharm. Bull. 2006, 29:2123.
37. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Mol. Brain Res. 1998, 57:1-9.
38. Johnson L.V., Walsh M.L., Chen L.B. Localization of mitochondria in living cells with rhodamine 123. Proc. Natl. Acad. Sci. 1980, 77:990-994.
39. Junghans A., Sies H., Stahl W. Macular pigments lutein and zeaxanthin as blue light filters studied in liposomes. Arch. Biochem. Biophys. 2001, 391:160-164.
40. Kageyama G.H., Wong-Riley M. The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey, with particular reference to retinal mosaics and ON/OFF-center visual channels. J.Neurosci. 1984, 4:2445-2459.
41. Kiffin R., Bandyopadhyay U., Cuervo A.M. Oxidative stress and autophagy. Antioxid. Redox Signal. 2006, 8:152-162.
42. Kuroiwa S., Katai N., Shibuki H., Kurokawa T., Umihira J., Nikaido T., Kametani K., Yoshimura N. Expression of cell cycle-related genes in dying cells in retinal ischemic injury. Investig. Ophthalmol. Vis. Sci. 1998, 39:610-617.
43. Larsen A.K., Osborne N.N. Involvement of adenosine in retinal ischemia. Studies on the rat. Investig. Ophthalmol. Vis. Sci. 1996, 37:2603-2611.
44. Lemasters J.J. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 2005, 8:3-5.
45. Li S.-Y., Lo A.C.Y. Lutein protects RGC-5 cells against hypoxia and oxidative stress. Int. J. Mol. Sci. 2010, 11:2109-2117.
46. Li S.-Y., Fu Z.-J., Ma H., Jang W.-C., So K.-F., Wong D., Lo A.C.Y. Effect of lutein on retinal neurons and oxidative stress in a model of acute retinal ischemia/reperfusion. Investig. Ophthalmol. Vis. Sci. 2009, 50:836-843.
47. Li S.-Y., Fung F.K.C., Fu Z.J., Wong D., Chan H.H.L., Lo A.C.Y. Anti-inflammatory effects of lutein in retinal ischemic/hypoxic Injury: invivo and invitro studies. Investig. Ophthalmol. Vis. Sci. 2012, 53:5976-5984.
48. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
49. Liu Q., Ju W.-K., Crowston J.G., Xie F., Perry G., Smith M.A., Lindsey J.D., Weinreb R.N. Oxidative stress is an early event in hydrostatic pressure-induced retinal ganglion cell damage. Investig. Ophthalmol. Vis. Sci. 2007, 48:4580-4589.
50. Maher P., Hanneken A. Flavonoids protect retinal ganglion cells from ischemia invitro. Exp. Eye Res. 2008, 86:366-374.
51. Mitchell J.B., Krishna M.C., Kuppusamy P., Cook J.A., Russo A. Protection against oxidative stress by nitroxides. Exp. Biol. Med. 2001, 226:620-621.
52. Mitchell P., Leung H., Wang J.J., Rochtchina E., Lee A.J., Wong T.Y., Klein R. Retinal vessel diameter and open-angle glaucoma: the Blue Mountains Eye Study. Ophthalmology 2005, 112:245-250.
53. Morrow B.J., Keddie D.J., Gueven N., Lavin M.F., Bottle S.E. Anovel profluorescent nitroxide as a sensitive probe for the cellular redox environment. Free Radic. Biol. Med. 2010, 49:67-76.
54. Moxon-Lester L., Takamoto K., Colditz P.B., Barnett N.L. S-Adenosyl-l-methionine restores photoreceptor function following acute retinal ischemia. Vis. Neurosci. 2009, 26:429-441.
55. Muriach M., Bosch-Morell F., Alexander G., Blomhoff R., Barcia J., Arnal E., Almansa I., Romero F.J., Miranda M. Lutein effect on retina and hippocampus of diabetic mice. Free Radic. Biol. Med. 2006, 41:979-984.
56. Nakajima Y., Shimazawa M., Otsubo K., Ishibashi T., Hara H. Zeaxanthin, a retinal carotenoid, protects retinal cells against oxidative stress. Curr. Eye Res. 2009, 34:311-318.
57. Naskar R., Wissing M., Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Investig. Ophthalmol. Vis. Sci. 2002, 43:2962-2968.
58. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J.Clin. Investig. 2003, 111:769-778.
59. Oharazawa H., Igarashi T., Yokota T., Fujii H., Suzuki H., Machide M., Takahashi H., Ohta S., Ohsawa I. Protection of the retina by rapid diffusion of hydrogen: administration of hydrogen-loaded eye drops in retinal ischemia-reperfusion injury. Investig. Ophthalmol. Vis. Sci. 2010, 51:487-492.
60. Osborne N.N. Pathogenesis of ganglion "cell death" in glaucoma and neuroprotection: focus on ganglion cell axonal mitochondria. Progress in Brain Research 2008, 339-352. Elsevier. L.C.N.N.O. Carlo Nucci, B. Giacinto (Eds.).
61. Osborne N.N., del Olmo-Aguado S. Maintenance of retinal ganglion cell mitochondrial functions as a neuroprotective strategy in glaucoma. Curr. Opin. Pharmacol. 2013, 13:16-22.
62. Osborne N.N., Casson R.J., Wood J.P.M., Chidlow G., Graham M., Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog. Retin. Eye Res. 2004, 23:91-147.
63. Pellegrini-Giampietro D.E., Cherici G., Alesiani M., Carla V., Moroni F. Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemia-induced neuronal damage. J.Neurosci. 1990, 10:1035-1041.
64. Penn R., Hagins W. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 1969, 223:201-204.
65. Ray A., Martinez B., Berkowitz L., Caldwell G., Caldwell K. Mitochondrial dysfunction, oxidative stress, and neurodegeneration elicited by a bacterial metabolite in a C. elegans Parkinson's model. Cell Death Dis. 2014, 5:e984.
66. Richer S., Stiles W., Statkute L., Pulido J., Frankowski J., Rudy D., Pei K., Tsipursky M., Nyland J. Double-masked, placebo-controlled, randomized trial of lutein and antioxidant supplementation in the intervention of atrophic age-related macular degeneration: the Veterans LAST study (Lutein Antioxidant Supplementation Trial). Optom. J. Am. Optom. Assoc. 2004, 75:216-229.
67. Richer S., Devenport J., Lang J.C. LAST II: differential temporal responses of macular pigment optical density in patients with atrophic age-related macular degeneration to dietary supplementation with xanthophylls. Optom. J. Am. Optom. Assoc. 2007, 78:213-219.
68. Robson J., Frishman L. Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis. Neurosci. 1995, 12:837-850.
69. Robson J.G., Frishman L.J. Dissecting the dark-adapted electroretinogram. Doc. Ophthalmol. 1998, 95:187-215.
70. Sasaki M., Ozawa Y., Kurihara T., Noda K., Imamura Y., Kobayashi S., Ishida S., Tsubota K. Neuroprotective effect of an antioxidant, lutein, during retinal inflammation. Investig. Ophthalmol. Vis. Sci. 2009, 50:1433-1439.
71. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 2007, 17:422-427.
72. Scherz-Shouval R., Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 2011, 36:30-38.
73. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007, 26:1749-1760.
74. Schwarz K., Siddiqi N., Singh S., Neil C.J., Dawson D.K., Frenneaux M.P. The breathing heart-mitochondrial respiratory chain dysfunction in cardiac disease. Int. J. Cardiol. 2014, 171:134-143.
75. Seo S.-j., Krebs M.P., Mao H., Jones K., Conners M., Lewin A.S. Pathological consequences of long-term mitochondrial oxidative stress in the mouse retinal pigment epithelium. Exp. Eye Res. 2012, 101:60-71.
76. Sieving P.A., Murayama K., Naarendorp F. Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave. Vis. Neurosci. 1994, 11:519-532.
77. Smith R.A.J., Adlam V.J., Blaikie F.H., Manas A.-R.B., Porteous C.M., James A.M., Ross M.F., Logan A., Cochemé H.M., Trnka J., Prime T.A., Abakumova I., Jones B.A., Filipovska A., Murphy M.P. Mitochondria-targeted antioxidants in the treatment of disease. Ann. N. Y. Acad. Sci. 2008, 1147:105-111.
78. Streit W.J., Graeber M.B., Kreutzberg G.W. Functional plasticity of microglia: a review. Glia 1988, 1:301-307.
79. Sun M.-H., Pang J.-H.S., 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.
80. Swartz H.M. Use of nitroxides to measure redox metabolism in cells and tissues. J.Chem. Soc. Faraday Trans. 1 Phys. Chem. Condens. Phases 1987, 83:191-202.
81. Swartz H.M. Principles of the metabolism of nitroxides and their implications for spin trapping. Free Radic. Res. Commun. 1990, 9:399-405.
82. Tezel G. Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog. Retin. Eye Res. 2006, 25:490-513.
83. Wachtmeister L., Dowling J.E. The oscillatory potentials of the mudpuppy retina. Investig. Ophthalmol. Vis. Sci. 1978, 17:1176-1188.
84. Wang X., Tay S.S.-W., Ng Y.-K. An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp. Brain Res. 2000, 132:476-484.
85. Wang B., Li P., Yu F., Chen J., Qu Z., Han K. Anear-infrared reversible and ratiometric fluorescent probe based on Se-BODIPY for the redox cycle mediated by hypobromous acid and hydrogen sulfide in living cells. Chem. Commun. 2013, 49:5790-5792.
86. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic. Biol. Med. 2007, 43:995-1022.
87. Wen-Xue Q., Xu W. Progress on fluorescent probes for reversible redox cycles and their application in living cell imaging. Chin. J. Anal. Chem. 2012, 40:1301.
88. Wilkinson-Berka J.L., Rana I., Armani R., Agrotis A. Reactive oxygen species, Nox and angiotensin II in angiogenesis: implications for retinopathy. Clin. Sci. 2013, 124:597-615.
89. Xu K., Qiang M., Gao W., Su R., Li N., Gao Y., Xie Y., Kong F., Tang B. Anear-infrared reversible fluorescent probe for real-time imaging of redox status changes invivo. Chem. Sci. 2013, 4:1079-1086.
90. Yapici N.B., Jockusch S., Moscatelli A., Mandalapu S.R., Itagaki Y., Bates D.K., Wiseman S., Gibson K.M., Turro N.J., Bi L. New rhodamine nitroxide based fluorescent probes for intracellular hydroxyl radical identification in living cells. Org. Lett. 2011, 14:50-53.
91. Yuki K., Ozawa Y., Yoshida T., Kurihara T., Hirasawa M., Ozeki N., Shiba D., Noda K., Ishida S., Tsubota K. Retinal ganglion cell loss in superoxide dismutase 1 deficiency. Investig. Ophthalmol. Vis. Sci. 2011, 52:4143-4150.