Optical imaging of mitochondrial redox state in rodent model of retinitis pigmentosa

Journal of Biomedical Optics

Volumn 18, Issue 1, 2013, Pages

  Maleki, Sepideh ^a   Gopalakrishnan, Sandeep ^b   Ghanian, Zahra ^a   Sepehr, Reyhaneh ^a   Schmitt, Heather ^b   Eells, Janis ^b   Ranji, Mahsa ^a  

^a University of Wisconsin Milwaukee   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Flavin adenine dinucleotide; Inherited retinal degeneration; Mitochondrial dysfunction; Nicotinamide adenine dinucleotide; Nicotinamide adenine dinucleotide redox ratio; Optical imaging; Oxidative stress

Indexed keywords

FLAVIN ADENINE DINUCLEOTIDE; MITOCHONDRIAL DYSFUNCTION; NICOTINAMIDE ADENINE DINUCLEOTIDES; OPTICAL IMAGING; REDOX RATIO; RETINAL DEGENERATIONS;

AMIDES; FLUORESCENCE; IMAGING TECHNIQUES; METABOLISM; OPHTHALMOLOGY; OPTICAL IMAGE STORAGE; OXIDATIVE STRESS; RATS; VISION;

FLUOROPHORES;

NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; DISEASE MODEL; FLUORESCENCE IMAGING; IMAGE PROCESSING; METABOLISM; METHODOLOGY; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; RAT; RETINITIS PIGMENTOSA; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; IMAGE PROCESSING, COMPUTER-ASSISTED; MITOCHONDRIA; NAD; OPTICAL IMAGING; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RETINITIS PIGMENTOSA;

MLCS; MLOWN;

EID: 84878225544     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.JBO.18.1.016004     Document Type: Article

References (65)

1. D. Besch et al., "Inherited multifocal RPE-diseases: mechanisms for local dysfunction in global retinoid cycle gene defects," Vision Res. 43(28), 3095-3108 (2003). (Pubitemid 37377623)
2. J. Sancho-Pelluz et al., "Photoreceptor cell death mechanisms in inherited retinal degeneration," Mol. Neurobiol. 38(3), 253-269 (2008).
3. D. T. Hartong, E. L. Berson, and T. P. Dryja, "Retinitis pigmentosa," Lancet 368(9549), 1795-1809 (2006). (Pubitemid 44739028)
4. K. Neveling et al., "Next-generation genetic testing for retinitis pigmentosa," Hum. Mutat. 33(6), 963-972 (2012).
5. T. P. Dryja et al., "Mutations within the rhodopsin gene in patients with autosomal dominant retinitis pigmentosa," N. Engl. J. Med. 323(19), 1302-1307 (1990). (Pubitemid 20364737)
6. M. Haeri and B. E. Knox, "Rhodopsin mutant P23H destabilizes rod photoreceptor disk membranes," PLoS One 7(1), e30101 (2012).
7. A. N. Bramall et al., "The genomic, biochemical, and cellular responses of the retina in inherited photoreceptor degenerations and prospects for the treatment of these disorders," Annu. Rev. Neurosci. 33, 441-472 (2010).
8. M. K. Shigenaga, T. M. Hagen, and B. N. Ames, "Oxidative damage and mitochondrial decay in aging," Proc. Natl. Acad. Sci. U. S. A. 91(23), 10771-10778 (1994). (Pubitemid 24349567)
9. D. C. Wallace, "A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine," Annu. Rev. Genet. 39(1), 359-407 (2005). (Pubitemid 43011120)
10. P. P. Karunadharma et al., "Mitochondrial DNA damage as a potential mechanism for age-related macular degeneration," Invest. Ophthalmol. Vis. Sci. 51(11), 5470-5479 (2010).
11. K. Green, M. D. Brand, and M. P. Murphy, "Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes," Diabetes 53(Suppl 1), S110-S118 (2004). (Pubitemid 38168702)
12. M. Ranji et al., "Fluorescence spectroscopy and imaging of myocardial apoptosis," J. Biomed. Opt. 11(6), 064036 (2006).
13. D. Vlachantoni et al., "Evidence of severe mitochondrial oxidative stress and a protective effect of low oxygen in mouse models of inherited photoreceptor degeneration," Hum. Mol. Genet. 20(2), 322-335 (2011).
14. N. Sanvicens et al., "Oxidative stress-induced apoptosis in retinal photoreceptor cells is mediated by calpains and caspases and blocked by the oxygen radical scavenger CR-6," J. Biol. Chem. 279(38), 39268-39278 (2004). (Pubitemid 39258188)
15. M. M. Sanz et al., "Significant photoreceptor rescue by treatment with a combination of antioxidants in an animal model for retinal degeneration," Neuroscience 145(3), 1120-1129 (2007). (Pubitemid 46463933)
16. M. Donovan, R. J. Carmody, and T. G. Cotter, "Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent," J. Biol. Chem. 276(25), 23000-23008 (2001).
17. H. Yamada et al., "Fibroblast growth factor-2 decreases hyperoxiainduced photoreceptor cell death in mice," Am. J. Pathol. 159(3), 1113-1120 (2001). (Pubitemid 32847202)
18. G. Y. Kong et al., "Mitochondrial dysfunction and glaucoma," J. Glaucoma. 18(2), 93-100 (2009).
19. S. R. Pieczenik and J. Neustadt, "Mitochondrial dysfunction and molecular pathways of disease," Exp. Mol. Pathol. 83(1), 84-92 (2007). (Pubitemid 46842959)
20. M. T. Lin and M. F. Beal, "Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases," Nature 443(7113), 787-795 (2006). (Pubitemid 44622683)
21. N. Ramanujam et al., "Low temperature fluorescence imaging of freezetrapped human cervical tissues," Opt. Express 8(6), 335-343 (2001).
22. S. Maleki et al., "Mitochondrial redox studies of oxidative stress in kidneys from diabetic mice," Biomed. Opt. Express 3(2), 273-281 (2012).
23. M. Ranji et al., "Quantifying acute myocardial injury using ratiometric fluorometry," IEEE Trans. Biomed. Eng. 56(5), 1556-1563 (2009).
24. R. Sepehr et al., "Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress," J. Biomed. Opt. 17(4), 046010 (2012).
25. M. Ranji et al., "Simultaneous fluorometry and phosphorometry of Langendorff perfused rat heart: ex vivo animal studies," Opt. Lett. 31(20), 2995-2997 (2006). (Pubitemid 44664587)
26. M. Matsubara et al., "In vivo fluorometric assessment of cyclosporine on mitochondrial function during myocardial ischemia and reperfusion," Ann. Thorac. Surg. 89(5), 1532-1537 (2010).
27. S. L. Bernard et al., "High spatial resolution measurements of organ blood flow in small laboratory animals," Am. J. Physiol. Heart Circ. Physiol. 279(5), H2043-H2052 (2000).
28. D. Y. Yu and S. J. Cringle, "Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease," Prog. Retin. Eye Res. 20(2), 175-208 (2001). (Pubitemid 32153715)
29. D. S. Cassarino et al., "Cyclosporin A increases resting mitochondrial membrane potential in SY5Y cells and reverses the depressed mitochondrial membrane potential of Alzheimer's disease cybrids," Biochem. Biophys. Res. Commun. 248(1), 168-173 (1998). (Pubitemid 28418206)
30. S. Machida et al., "P23H rhodopsin transgenic rat: correlation of retinal function with histopathology," Invest. Ophthalmol. Vis. Sci. 41(10), 3200-3209 (2000).
31. Z. Ghanian et al., "Optical imaging of oxidative stress in diabetic retinopathy," in Biomedical Engineering Society, Atlanta (2012).
32. F. C. Delori et al., "Monochromatic ophthalmoscopy and fundus photography. The normal fundus," Arch. Ophthalmol. 95(5), 861-868 (1977). (Pubitemid 8257574)
33. G. A. Williams et al., "Single-field fundus photography for diabetic retinopathy screening: a report by the American Academy of Ophthalmology," Ophthalmology 111(5), 1055-1062 (2004). (Pubitemid 38586705)
34. R. H.Webb and G.W. Hughes, "Scanning laser ophthalmoscope," IEEE Trans. Biomed. Eng. 28(7), 488-492 (1981). (Pubitemid 11009533)
35. D. Huang et al., "Optical coherence tomography," Science 254(5035), 1178-1181 (1991). (Pubitemid 21917444)
36. M. Wojtkowski et al., "In vivo human retinal imaging by Fourier domain optical coherence tomography," J. Biomed. Opt. 7(3), 457-463 (2002).
37. N. Nassif et al., "In vivo high-resolution video-rate spectral-domain optical coherence tomography of the human retina and optic nerve," Opt. Express 12(3), 367-376 (2004).
38. M. Ruggeri et al., "In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 48(4), 1808-1814 (2007). (Pubitemid 351261369)
39. A. Harris et al., "A review of methods for human retinal oximetry," Ophthalmic Surg. Laser. Imag. 34(2), 152-164 (2003). (Pubitemid 36723161)
40. M. Hammer et al., "Light paths in retinal vessel oxymetry," IEEE Trans. Biomed. Eng. 48(5), 592-598 (2001). (Pubitemid 32378060)
41. H. F. Zhang, K. Maslov, and L. V. Wang, "In vivo imaging of subcutaneous structures using functional photoacoustic microscopy," Nat. Protoc. 2(4), 797-804 (2007). (Pubitemid 46745576)
42. H. F. Zhang et al., "Functional photoacoustic microscopy for highresolution and noninvasive in vivo imaging," Nat. Biotechnol. 24(7), 848-851 (2006). (Pubitemid 44086627)
43. K. Maslov et al., "Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries," Opt. Lett. 33(9), 929-931 (2008).
44. M. H. Smith et al., "Oxygen saturation measurements of blood in retinal vessels during blood loss," J. Biomed. Opt. 3(3), 296-303 (1998). (Pubitemid 128635003)
45. D. Schweitzer et al., "A new method for the measurement of oxygen saturation at the human ocular fundus," Int. Ophthalmol. 23(4-6), 347-353 (2001). (Pubitemid 34256601)
46. M. Hammer and D. Schweitzer, "Quantitative reflection spectroscopy at the human ocular fundus," Phys. Med. Biol. 47(2), 179-191 (2002). (Pubitemid 34110607)
47. K. R. Denninghoff et al., "Retinal venous oxygen saturation and cardiac output during controlled hemorrhage and resuscitation," J. Appl. Physiol. 94(3), 891-896 (2003). (Pubitemid 36232000)
48. R. D. Shonat et al., "Oxygen distribution in the retinal and choroidal vessels of the cat as measured by a new phosphorescence imaging method," Appl. Opt. 31(19), 3711-3718 (1992).
49. R. D. Shonat and A. C. Kight, "Oxygen tension imaging in the mouse retina," Ann. Biomed. Eng. 31(9), 1084-1096 (2003).
50. P.W. Ferrez et al., "Effect of visual stimulation on blood oxygenation in the optic nerve head of miniature pigs: a pilot study," Klin. Monbl. Augenheilkd. 221(5), 364-366 (2004). (Pubitemid 38807955)
51. Y. Ito and B. A. Berkowitz, "MR studies of retinal oxygenation," Vision Res. 41(10-11), 1307-1311 (2001). (Pubitemid 32367892)
52. R. Roberts et al., "Spatial pattern and temporal evolution of retinal oxygenation response in oxygen-induced retinopathy," Invest. Ophthalmol. Vis. Sci. 44(12), 5315-5320 (2003). (Pubitemid 37475404)
53. N. D. Wangsa-Wirawan and R. A. Linsenmeier, "Retinal oxygen: fundamental and clinical aspects," Arch. Ophthalmol. 121(4), 547-557 (2003). (Pubitemid 36427642)
54. M. Shahidi et al., "Three-dimensional mapping of chorioretinal vascular oxygen tension in the rat," Invest. Ophthalmol. Vis. Sci. 50(2), 820-825 (2009).
55. A. Shakoor et al., "Chorioretinal vascular oxygen tensiochanges in response to light flicker," Invest. Ophthalmol. Vis. Sci. 47(11), 4962-4965 (2006). (Pubitemid 46586400)
56. J. L. Dunaief et al., "The role of apoptosis in age-related macular degeneration," Arch. Ophthalmol. 120(11), 1435-1442 (2002). (Pubitemid 36406417)
57. F. Podesta et al., "Bax is increased in the retina of diabetic subjects and is associated with pericyte apoptosis in vivo and in vitro," Am. J. Pathol. 156(3), 1025-1032 (2000). (Pubitemid 30626960)
58. L. A. Kerrigan et al., "TUNEL-positive ganglion cells in human primary open-angle glaucoma," Arch. Ophthalmol. 115(8), 1031-1035 (1997). (Pubitemid 27328493)
59. Y. Du, C. M. Miller, and T. S. Kern, "Hyperglycemia increases mitochondrial superoxide in retina and retinal cells," Free Radic. Biol. Med. 35(11), 1491-1499 (2003). (Pubitemid 37452474)
60. A. Kindzelskii and H. R. Petty, "Fluorescence spectroscopic detection of mitochondrial flavoprotein redox oscillations and transient reduction of the NADPH oxidase-associated flavoprotein in leukocytes," Eur. Biophys. J. 33(4), 291-299 (2004). (Pubitemid 38915616)
61. K. C. Reinert et al., "Flavoprotein autofluorescence imaging of neuronal activation in the cerebellar cortex in vivo," J. Neurophysiol. 92(1), 199-211 (2004). (Pubitemid 38802244)
62. V. M. Elner et al., "Flavoprotein autofluorescence detection of early ocular dysfunction," Arch. Ophthalmol. 126(2), 259-260 (2008). (Pubitemid 351240857)
63. M. G. Field et al., "Rapid, noninvasive detection of diabetes-induced retinal metabolic stress," Arch. Ophthalmol. 126(7), 934-938 (2008). (Pubitemid 352008373)
64. S. G. Elner et al., "Retinal flavoprotein autofluorescence as a measure of retinal health," Trans. Am. Ophthalmol. Soc. 106, 215-222 (2008).
65. T. Liu et al., "Combined photoacoustic microscopy and optical coherence tomography can measure metabolic rate of oxygen," Biomed. Opt. Express 2(5), 1359-1365 (2011).