In vivo imaging of retinal oxidative stress using a reactive oxygen species-activated fluorescent probe

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 10, 2015, Pages 5862-5870

  Prunty, Megan C ^a   Aung, Moe H ^a   Hanif, Adam M ^b   Allen, Rachael S ^b   Chrenek, Micah A ^a   Boatright, Jeffrey H ^a,b   Thule, Peter M ^a,c   Kundu, Kousik ^d   Murthy, Niren ^e   Pardue, Machelle T ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Atlanta VA Center for Visual and Neurocognitive Rehabilitation ^*  (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

^d LI COR BIOSCIENCES   (United States)

^e University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; BIOLOGICAL MARKER; REACTIVE OXYGEN METABOLITE;

AGE RELATED MACULAR DEGENERATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DIABETIC RETINOPATHY; DIAGNOSTIC IMAGING; ELECTRORETINOGRAPHY; FLUORESCENCE MICROSCOPY; GLAUCOMA; HISTOPATHOLOGY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RETINA DEGENERATION; RETINA INJURY; SCANNING LASER OPHTHALMOSCOPY; ANIMAL; DISEASE MODEL; DOSE RESPONSE; LONG EVANS RAT; METABOLISM; OPHTHALMOSCOPY; PHYSIOLOGY; PROCEDURES; RAT;

ANIMALS; BIOMARKERS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT DYES; MICE; MICROSCOPY, FLUORESCENCE; OPHTHALMOSCOPY; OXIDATIVE STRESS; RATS; RATS, LONG-EVANS; REACTIVE OXYGEN SPECIES; RETINAL DEGENERATION;

EID: 84941340742     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-16810     Document Type: Article

References (55)

1. Blasiak J, Petrovski G, Vereb Z, Facsko A, Kaarniranta K. Oxidative stress, hypoxia, and autophagy in the neovascular processes of age-related macular degeneration. Biomed Res Int. 2014;2014:768026.
2. Kiang AS, Humphries MM, Campbell M, Humphries P. Antioxidant therapy for retinal disease. Adv Exp Med Biol. 2014;801:783-789.
3. Pinazo-Duran MD, Zanon-Moreno V, Garcia-Medina JJ, Gallego-Pinazo R. Evaluation of presumptive biomarkers of oxidative stress, immune response and apoptosis in primary open-angle glaucoma. Curr Opin Pharmacol. 2013;13:98-107.
4. Elahy M, Baindur-Hudson S, Cruzat VF, Newsholme P, Dass CR. Mechanisms of PEDF-mediated protection against reactive oxygen species damage in diabetic retinopathy and neuropa- thy. J Endocrinol. 2014;222:R129-R139.
5. Williams M, Hogg RE, Chakravarthy U. Antioxidants and diabetic retinopathy. Curr Diab Rep. 2013;13:481-487.
6. Payne AJ, Kaja S, Naumchuk Y, Kunjukunju N, Koulen P. Antioxidant drug therapy approaches for neuroprotection in chronic diseases of the retina. Int J Mol Sci. 2014;15:1865-1886.
7. Maleki S, Gopalakrishnan S, Ghanian Z, et al. Optical imaging of mitochondrial redox state in rodent model of retinitis pigmentosa. J Biomed Opt. 2013;18:16004.
8. Kutty RK, Kutty G, Wiggert B, Chader GJ, Darrow RM, Organisciak DT. Induction of heme oxygenase 1 in the retina by intense visible light: suppression by the antioxidant dimethylthiourea. Proc Natl Acad Sci U S A. 1995;92:1177-1181.
9. Organisciak DT, Vaughan DK. Retinal light damage: mecha-nisms and protection. Prog Retin Eye Res. 2010;29:113-134.
10. Pinazo-Duran MD, Gallego-Pinazo R, Garcia-Medina JJ, et al. Oxidative stress and its downstream signaling in aging eyes. Clin Interv Aging. 2014;9:637-652.
11. Komeima K, Rogers BS, Campochiaro PA. Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa. J Cell Physiol. 2007;213:809-815.
12. Boatright JH, Moring AG, McElroy C, et al. Tool from ancient pharmacopoeia prevents vision loss. Mol Vis. 2006;12:1706-1714.
13. Osborne NN, del Olmo-Aguado S. Maintenance of retinal ganglion cell mitochondrial functions as a neuroprotective strategy in glaucoma. Curr Opin Pharmacol. 2013;13:16-22.
14. Lee D, Kim KY, Shim MS, et al. Coenzyme Q10 ameliorates oxidative stress and prevents mitochondrial alteration in ischemic retinal injury. Apoptosis. 2014;19:603-614.
15. Pitocco D, Tesauro M, Alessandro R, Ghirlanda G, Cardillo C. Oxidative stress in diabetes: implications for vascular and other complications. Int J Mol Sci. 2013;14:21525-21550.
16. Liu Q, Ju WK, Crowston JG, et al. Oxidative stress is an early event in hydrostatic pressure induced retinal ganglion cell damage. Invest Ophthalmol Vis Sci. 2007;48:4580-4589.
17. Du Y, Veenstra A, Palczewski K, Kern TS. Photoreceptor cells are major contributors to diabetes-induced oxidative stress and local inflammation in the retina. Proc Natl Acad Sci U S A. 2013;110:16586-16591.
18. Arden GB, Sivaprasad S. The pathogenesis of early retinal changes of diabetic retinopathy. Doc Ophthalmol. 2012;124: 15-26.
19. Frost SM, Kanagasingam Y, Macaulay SL. Ocular biomarkers for neurodegenerative and systemic disease. Med J Aust. 2014; 201:128.
20. Schoknecht K, Prager O, Vazana U, et al. Monitoring stroke progression: in vivo imaging of cortical perfusion, blood-brain barrier permeability and cellular damage in the rat photo- thrombosis model. J Cereb Blood Flow Metab. 2014;34:1791-1801.
21. Allen RS, Sayeed I, Cale HA, et al. Severity of middle cerebral artery occlusion determines retinal deficits in rats. Exp Neurol. 2014;254:206-215.
22. Frost S, Martins RN, Kanagasingam Y. Ocular biomarkers for early detection of Alzheimer’s disease. J Alzheimers Dis. 2010; 22:1-16.
23. Tas A, Yolcu U, Ilhan A, Gundogan FC. Detection of retinal nerve fibre layer degeneration in patients with Alzheimer’s disease using optical coherence tomography: searching new biomarkers (published online ahead of print December 9, 2014). Acta Ophthalmol. doi:10.1111/aos.12614.
24. Blake R, Trounce IA. Mitochondrial dysfunction and compli-cations associated with diabetes. Biochim Biophys Acta. 2014; 1840:1404-1412.
25. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol. 2007;8:722-728.
26. Park SW, Cho CS, Jun HO, et al. Anti-angiogenic effect of luteolin on retinal neovascularization via blockade of reactive oxygen species production. Invest Ophthalmol Vis Sci. 2012; 53:7718-7726.
27. Zielonka J, Vasquez-Vivar J, Kalyanaraman B. Detection of 2-hydroxyethidium in cellular systems: a unique marker product of superoxide and hydroethidine. Nat Protoc. 2008;3:8-21.
28. Pritsos CA, Constantinides PP, Tritton TR, Heimbrook DC, Sartorelli AC. Use of high-performance and superoxide liquid chromatography to detect hydroxyl radicals generated from mitomycin C. Anal Biochem. 1985;150:294-299.
29. Rayner CL, Gole GA, Bottle SE, Barnett NL. Dynamic, in vivo, real-time detection of retinal oxidative status in a model of elevated intraocular pressure using a novel, reversibly responsive, profluorescent nitroxide probe. Exp Eye Res. 2014;129:48-56.
30. Kundu K, Knight SF, Willett N, Lee S, Taylor WR, Murthy N. Hydrocyanines: a class of fluorescent sensors that can image reactive oxygen species in cell culture, tissue, and in vivo. Angew Chem Int Ed Engl. 2009;48:299-303.
31. Lin PW, Myers LE, Ray L, et al. Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation. Free Radic Biol Med. 2009;47:1205-1211.
32. Willett NJ, Kundu K, Knight SF, Dikalov S, Murthy N, Taylor WR. Redox signaling in an in vivo murine model of low magnitude oscillatory wall shear stress. Antioxid Redox Signal. 2011;15:1369-1378.
33. Dinjaski N, Fernandez-Gutierrez M, Selvam S, et al. PHACOS, a functionalized bacterial polyester with bactericidal activity against methicillin-resistant Staphylococcus aureus. Biomate- rials. 2014;35:14-24.
34. Selvam S, Kundu K, Templeman KL, Murthy N, Garcia AJ. Minimally invasive, longitudinal monitoring of biomaterial-associated inflammation by fluorescence imaging. Biomateri- als. 2011;32:7785-7792.
35. Suri S, Lehman SM, Selvam S, et al. In vivo fluorescence imaging of biomaterial-associated inflammation and infection in a minimally invasive manner. J Biomed Mater Res A. 2015; 103:76-83.
36. Magalotti S, Gustafson TP, Cao Q, et al. Evaluation of inflammatory response to acute ischemia using near-infrared fluorescent reactive oxygen sensors. Mol Imaging Biol. 2013; 15:423-430.
37. Goodson P, Kumar A, Jain L, et al. Nadph oxidase regulates alveolar epithelial sodium channel activity and lung fluid balance in vivo via O(-)(2) signaling. Am J Physiol Lung Cell Mol Physiol. 2012;302:L410-L419.
38. Kim JY, Choi WI, Kim YH, Tae G. Highly selective in-vivo imaging of tumor as an inflammation site by ROS detection using hydrocyanine-conjugated, functional nano-carriers. J Control Release. 2011;156:398-405.
39. Xie L, Lin AS, Kundu K, Levenston ME, Murthy N, Guldberg RE. Quantitative imaging of cartilage and bone morphology, reactive oxygen species, and vascularization in a rodent model of osteoarthritis. Arthritis Rheum. 2012;64:1899-1908.
40. Kundu K, Knight SF, Lee S, Taylor WR, Murthy N. A significant improvement of the efficacy of radical oxidant probes by the kinetic isotope effect. Angew Chem Int Ed Engl. 2010;49: 6134-6138.
41. Demontis GC, Longoni B, Marchiafava PL. Molecular steps involved in light-induced oxidative damage to retinal rods. Invest Ophthalmol Vis Sci. 2002;43:2421-2427.
42. Turner PV, Albassam MA. Susceptibility of rats to corneal lesions after injectable anesthesia. Comp Med. 2005;55:175-182.
43. Guillet R, Wyatt J, Baggs RB, Kellogg KC. Anesthetic-induced corneal lesions in developmentally sensitive rats. Invest Ophthalmol Vis Sci. 1988;29:6:949-954.
44. Seeliger MW, Beck SC, Pereyra-Munoz N, et al. In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vision Res. 2005;45:3512-3519.
45. Prusky GT, Alam NM, Beekman S, Douglas RM. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci. 2004;45:4611-4616.
46. Prusky GT, West PW, Douglas RM. Behavioral assessment of visual acuity in mice and rats. Vision Res. 2000;40:2201-2209.
47. Aung MH, Kim MK, Olson DE, Thule PM, Pardue MT. Early visual deficits in streptozotocin-induced diabetic long evans rats. Invest Ophthalmol Vis Sci. 2013;54:1370-1377.
48. Aung MH, Park HN, Han MK, et al. Dopamine deficiency contributes to early visual dysfunction in a rodent model of type 1 diabetes. J Neurosci. 2014;34:726-736.
49. Lawson EC, Han MK, Sellers JT, et al. Aerobic exercise protects retinal function and structure from light-induced retinal degeneration. J Neurosci. 2014;34:2406-2412.
50. Mocko JA, Kim M, Faulkner AE, Cao Y, Ciavatta VT, Pardue MT. Effects of subretinal electrical stimulation in mer-KO mice. Invest Ophthalmol Vis Sci. 2011;52:4223-4230.
51. Munzel T. Detection of superoxide in vascular tissue. Arterioscler Thromb Vasc Biol. 2002;22:1761-1768.
52. Noell WK, Walker VS, Kang BS, Berman S. Retinal damage by light in rats. Invest Ophthalmol Vis Sci. 1966;5:450-473.
53. Kevany BM, Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda). 2010;25:8-15.
54. Zarebski M, Kordon M, Dobrucki JW. Photosensitized damage inflicted on plasma membranes of live cells by an extracellular generator of singlet oxygen—a linear dependence of a lethal dose on light intensity. Photochem Photobiol. 2014;90:709-715.
55. Marshall MV, Draney D, Sevick-Muraca EM, Olive DM. Single-dose intravenous toxicity study of IRDye 800CW in Sprague- Dawley rats. Mol Imaging Biol. 2010;12:583-594.