Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 5, 2013, Pages 3366-3377

  Miura, Yoko ^a   Huettmann, Gereon ^a   Orzekowsky Schroeder, Regina ^a   Steven, Philipp ^b   Szaszák, Márta ^a   Koop, Norbert ^a   Brinkmann, Ralf ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Fluorescence lifetime imaging; Laser photocoagulation; Oxidative stress; Retinal pigment epithelium; Two photon microscopy

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE; EMISSION SPECTROGRAPHY; EXCITATION SPECTRUM; FLUORESCENCE IMAGING; FLUORESCENCE LIFETIME IMAGING; FLUORESCENCE MICROSCOPY; HISTOLOGY; LIPID PEROXIDATION; MELANOSOME; NONHUMAN; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; SPECTRUM;

FLUORESCENCE LIFETIME IMAGING; LASER PHOTOCOAGULATION; OXIDATIVE STRESS; RETINAL PIGMENT EPITHELIUM; TWO PHOTON MICROSCOPY;

ANIMALS; CELLS, CULTURED; CHOROID; CYTOPLASMIC GRANULES; FERROUS COMPOUNDS; LASER COAGULATION; MELANOSOMES; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; PHOTONS; REACTIVE OXYGEN SPECIES; RETINAL PIGMENT EPITHELIUM; SWINE;

EID: 84877649817     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11808     Document Type: Article

References (53)

1. Schenke-Layland K, Riemann I, Damour O, Stock UA, Konig K. Two-photon microscopes and in vivo multiphoton tomographs-powerful diagnostic tools for tissue engineering and drug delivery. Adv Drug Deliv Rev. 2006;58:878-896.
2. Rubart M. Two-photon microscopy of cells and tissue. Circ Res. 2004;95:1154-1166.
3. Steven P, Müller M, Koop M, Rose C, Hüttmann G. Comparison of confocal and two-photon microscopy for non-invasive imaging of ocular surface pathologies. J Biomed Opt. 2009; 14:064040.
4. Gehlsen U, Hüttmann G, Steven P. Intravital multidimensional real-time imaging of the conjunctival immune system. Dev Ophthalmol. 2010;45:40-48.
5. Crosignani V, Dvornikov A, Aguilar JS, et al. Deep tissue fluorescence imaging and in vivo biological applications. J Biomed Opt. 2012;17:116023.
6. Cahalan MD, Parker I, Wei SH, Miller MJ. Two-photon tissue imaging: seeing the immune system in a fresh light. Nav Rev Immunol. 2002;2:872-880.
7. Mayevsky A, Rogatsky GG. Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am J Physiol Cell Physiol. 2007;292:C615-C640.
8. Thorell B. Flow-cytometric monitoring of intracellular flavins simultaneously with NAD(P)H levels. Cytometry. 1983;4:61-65.
9. Kiefer CR, McKenney JB, Trainor JF, et al. Porphyrin loading of lipofuscin granules in inflamed striated muscle. Am J Pathol. 1998;153:703-708.
10. Eldred GE, Miller GV, Stark WS, Feeney-Burns L. Lipofuscin: resolution of discrepant fluorescence data. Science. 1982;216: 757-759.
11. Gareau DS, Bargo PR, Horton WA, Jacques SL. Confocal fluorescence spectroscopy of subcutaneous cartilage expressing green fluorescent protein versus cutaneous collagen autofluorescence. J Biomed Opt. 2004;9:254-258.
12. Konig K, Schenke-Layland K, Riemann I, Stock UA. Multiphoton autofluorescence imaging of intratissue elastic fibers. Biomaterials. 2005;26:495-500.
13. Solbach U, Keilhauer C, Knabben H, Wolf S. Imaging of retinal autofluorescence in patients with age-related macular degeneration. Retina. 1997;17:385-389.
14. Delori FC, Dorey CK, Staurenghi G, Arend O, Goger DG, Weiter JJ. In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics. Invest Ophthalmol Vis Sci. 1995;36:718-729.
15. Matsumoto H, Kishi S, Sato T, Mukai R. Fundus autofluorescence of elongated photoreceptor outer segments in central serous chorioretinopathy. Am J Ophthalmol. 2011;151:617-623+e1.
16. Sekiryu T, Iida T, Maruko I, Saito K, Kondo T. Infrared fundus autofluorescence and central serous chorioretinopathy. Invest Ophthalmol Vis Sci. 2010;51:4956-4962.
17. Kellner U, Kellner S, Weinitz S. Fundus autofluorescence (488 NM) and near-infrared autofluorescence (787 NM) visualize different retinal pigment epithelium alterations in patients with age-related macular degeneration. Retina. 2010;30:6-15.
18. Peng XJ, Zhang WF. Lipofuscin- and melanin-related fundus autofluorescence in patients with submacular idiopathic choroidal neovascularization. Yan Ke Xue Bao. 2012;27:138-142.
19. Lakowicz JR, Szmacinski H, Nowaczyk K, Johnson ML. Fluorescence lifetime imaging of free and protein-bound NADH. Proc Natl Acad Sci U S A. 1992;89:1271-1275.
20. Tanaka F, Tamai N, Yamazaki I, Nakashima N, Yoshihara K. Temperature-induced changes in the coenzyme environment of D-amino acid oxidase revealed by the multiple decays of FAD fluorescence. Biophys J. 1989;56:901-909.
21. Szaszak M, Steven P, Shima K, et al. Fluorescence lifetime imaging unravels C. trachomatis metabolism and its crosstalk with the host cell. PLoS Pathog. 2011;7:e1002108.
22. Gehlsen U, Oetke A, Szaszak M, et al. Two-photon fluorescence lifetime imaging monitors metabolic changes during wound healing of corneal epithelial cells in vitro. Graefes Arch Clin Exp Ophthalmol. 2012;250:1293-1302.
23. Christen WG, Glynn RJ, Hennekens CH. Antioxidants and age related eye disease. Current and future perspectives. Ann Epidemiol. 1996;6:60-66.
24. Cai J, Nelson KC, Wu M, Sternberg P Jr, Jones DP. Oxidative damage and protection of the RPE. Prog Retin Eye Res. 2000; 19:205-221.
25. Chowers I, Wong R, Dentchev T, et al. The iron carrier transferrin is upregulated in retinas from patients with age related macular degeneration. Invest Ophthalmol Vis Sci. 2006;47:2135-2140.
26. Dunaief JL. Iron induced oxidative damage as a potential factor in age-related macular degeneration: the Cogan Lecture. Invest Ophthalmol Vis Sci. 2006;47:4660-4664.
27. Cleary CA, Jungkim S, Ravikumar K, Kelliher C, Acheson RW, Hickey-Dwyer M. Intravitreal bevacizumab in the treatment of neovascular age-related macular degeneration, 6- and 9-month results. Eye (Lond). 2008;22:82-86.
28. Muether PS, Hermann MM, Viebahn U, Kirchhof B, Fauser S. Vascular endothelial growth factor in patients with exudative age-related macular degeneration treated with ranibizumab. Ophthalmology. 2012;119:2082-2086.
29. Miura Y, Klettner A, Noelle B, Hasselbach H, Roider J. Change of morphological and functional characteristics of retinal pigment epithelium cells during cultivation of retinal pigment epithelium-choroid perfusion tissue culture. Ophthalmic Res. 2010;43:122-133.
30. Orzekowsky-Schroeder R, Klinger A, Martensen B, et al. In vivo spectral imaging of different cell types in the small intestine by two-photon excited autofluorescence. J Biomed Opt. 2011;16: 116025.
31. Becker W. Fluorescence lifetime imaging-techniques and applications. J Microsc. 2012;247:119-136.
32. Katz ML, Stientjes HJ, Gao CL, Christianson JS. Iron-induced accumulation of lipofuscin-like fluorescent pigment in the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1993; 34:3161-3171.
33. Katz ML, Christianson JS, Gao CL, Handelman GJ. Iron-induced fluorescence in the retina: dependence on vitamin A. Invest Ophthalmol Vis Sci. 1994;35:3613-3624.
34. Terrasa A, Guajardo M, Catala A. Lipoperoxidation of rod outer segments of bovine retina is inhibited by soluble binding proteins for fatty acids. Mol Cell Biochem. 1998;178:181-186.
35. Fagali N, Catala A. Fe2+ and Fe3+ initiated peroxidation of sonicated and non-sonicated liposomes made of retinal lipids in different aqueous media. Chem Phys Lipids. 2009;159:88-94.
36. Boulton M, Marshall J. Repigmentation of human retinal pigment epithelial cells in vitro. Exp Eye Res. 1985;41:209-218.
37. Peters S, Hammer M, Schweitzer D. Two-photon excited fluorescence microscopy application for ex vivo investigation of ocular fundus samples. Proc SPIE. 2011;8086:808605.
38. Teuchner K, Freyer W, Leupold D, et al. Femtosecond two photon excited fluorescence of melanin. Photochem Photobiol. 1999;70:146-151.
39. Dimitrow E, Riemann I, Ehlers A, et al. Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis. Exp Dermatol. 2009;18:509-515.
40. Katz ML, Shanker MJ. Development of lipofuscin-like fluorescence in the retinal pigment epithelium in response to protease inhibitor treatment. Mech Ageing Dev. 1989;49:23-40.
41. Kayatz P, Thumann G, Luther TT, et al. Oxidation causes melanin fluorescence. Invest Ophthalmol Vis Sci. 2001;42:241-246.
42. Imanishi Y, Batten ML, Piston DW, Baehr W, Palczewski K. Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J Cell Biol. 2004;164:373-383.
43. Palczewska G, Maeda T, Imanishi Y, et al. Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes. Nat Med. 2010; 16:1444-1449.
44. Han M, Bindewald-Wittich A, Holz FG, et al. Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells. J Biomed Opt. 2006;11:010501.
45. Eichhoff G, Busche MA, Garaschuk O. In vivo calcium imaging of the aging and diseased brain. Eur J Nucl Med Mol Imaging. 2008;35(suppl 1):S99-S106.
46. Bindewald-Wittich A, Han M, Schmitz-Valckenberg S, et al. Two-photon-excited fluorescence imaging of human RPE cells with a femtosecond Ti: Sapphire laser. Invest Ophthalmol Vis Sci. 2006;47:4553-4557.
47. Lamb LE, Simon JD. A2E: a component of ocular lipofuscin. Photochem Photobiol. 2004;79:127-136.
48. Framme C, Schule G, Birngruber R, et al. Temperature ependent fluorescence of A2-E, the main fluorescent lipofuscin component in the RPE. Curr Eye Res. 2004;29:287-291.
49. Cubeddu R, Taroni P, Hu DN, Sakai N, Nakanishi K, Roberts JE. Photophysical studies of A2-E, putative precursor of lipofuscin, in human retinal pigment epithelial cells. Photochem Photobiol. 1999;70:172-175.
50. Schweitzer D, Schenke S, Hammer M, et al. Towards metabolic mapping of the human retina. Microsc Res Tech. 2007;70:410-419.
51. Schweitzer D, Hammer M, Schweitzer F, et al. In vivo measurement of time-resolved autofluorescence at the human fundus. J Biomed Opt. 2004;9:1214-1222.
52. Schweitzer D, Quick S, Schenke S, et al. Comparison of parameters of time-resolved autofluorescence between healthy subjects and patients suffering from early AMD. Ophthalmologe. 2009;106:714-722.
53. Schweitzer D, Gaillard ER, Dillon J, et al. Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen. Invest Ophthalmol Vis Sci. 2012;53:3376-3386.