Lack of correlation between the spatial distribution of A2E and lipofuscin fluorescence in the human retinal pigment epithelium

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 8, 2013, Pages 5535-5542

  Ablonczy, Zsolt ^a   Higbee, Daniel ^b   Anderson, David M ^c   Dahrouj, Mohammad ^a   Grey, Angus C ^d   Gutierrez, Danielle ^e   Koutalos, Yiannis ^a   Schey, Kevin L ^c   Hanneken, Anne ^f   Crouch, Rosalie K ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b Vanderbilt University School of Medicine ^*

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e TEXAS A AND M UNIVERSITY CORPUS CHRISTI   (United States)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

A2E; Human; Imaging; Lipofuscin; Mass spectrometry; Retinal degeneration; Retinoids

Indexed keywords

A2E; LIPOFUSCIN; PIGMENT; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ARTICLE; CHILD; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN TISSUE; IMAGING; INFANT; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PIGMENT EPITHELIUM; PRIORITY JOURNAL;

A2E; HUMAN; IMAGING; LIPOFUSCIN; MASS SPECTROMETRY; RETINAL DEGENERATION; RETINOIDS;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; BIOLOGICAL MARKERS; CHILD; CHILD, PRESCHOOL; HUMANS; INFANT; INFANT, NEWBORN; LIPOFUSCIN; MIDDLE AGED; PYRIDINIUM COMPOUNDS; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; RETINOIDS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; YOUNG ADULT;

EID: 84882781321     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12250     Document Type: Article

References (36)

1. Sparrow JR, Gregory-Roberts E, Yamamoto K, et al. The bisretinoids of retinal pigment epithelium. Prog Retin Eye Res. 2012;31:121-135.
2. Sakai N, Decatur J, Nakanishi K, Eldred GE. Ocular age pigment "A2E": an unprecedented pyridinium bisretinoid. J Am Chem Soc. 1996;118:1559-1560.
3. 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.
4. Feeney L. Lipofuscin and melanin of human retinal pigment epithelium. Fluorescence, enzyme cytochemical, and ultrastructural studies. Invest Ophthalmol Vis Sci. 1978;17:583-600.
5. Wing GL, Blanchard GC, Weiter JJ. The topography and age relationship of lipofuscin concentration in the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1978;17:601-607.
6. Ng KP, Gugiu B, Renganathan K, et al. Retinal pigment epithelium lipofuscin proteomics. Mol Cell Proteomics. 2008; 7:1397-1405.
7. Liu J, Itagaki Y, Ben-Shabat S, Nakanishi K, Sparrow JR. The biosynthesis of A2E, a fluorophore of aging retina, involves the formation of the precursor, A2-PE, in the photoreceptor outer segment membrane. J Biol Chem. 2000;275:29354-29360.
8. Boyer NP, Higbee D, Currin MB, et al. Lipofuscin and Nretinylidene-N-retinylethanolamine (A2E) accumulate in retinal pigment epithelium in absence of light exposure: their origin is 11-cis-retinal. J Biol Chem. 2012;287:22276-22286.
9. Katz ML, Drea CM, Robison WG Jr. Relationship between dietary retinol and lipofuscin in the retinal pigment epithelium. Mech Ageing Dev. 1986;35:291-305.
10. Katz ML, Redmond TM. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2001;42: 3023-3030.
11. Maeda A, Maeda T, Imanishi Y, et al. Role of photoreceptorspecific retinol dehydrogenase in the retinoid cycle in vivo. J Biol Chem. 2005;280:18822-18832.
12. Murdaugh LS, Mandal S, Dill AE, Dillon J, Simon JD, Gaillard ER. Compositional studies of human RPE lipofuscin: mechanisms of molecular modifications. J Mass Spectrom. 2011;46: 90-95.
13. Mata NL, Weng J, Travis GH. Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc Natl Acad Sci U S A. 2000;97: 7154-7159.
14. Bakall B, Radu RA, Stanton JB, et al. Enhanced accumulation of A2E in individuals homozygous or heterozygous for mutations in BEST1 (VMD2). Exp Eye Res. 2007;85:34-43.
15. Wu Y, Fishkin NE, Pande A, Pande J, Sparrow JR. Novel lipofuscin bisretinoids prominent in human retina and in a model of recessive Stargardt disease. J Biol Chem. 2009;284: 20155-20166.
16. Sparrow JR, Kim SR, Cuervo AM, Bandhyopadhyayand U. A2E, a pigment of RPE lipofuscin, is generated from the precursor, A2PE by a lysosomal enzyme activity. Adv Exp Med Biol. 2008; 613:393-398.
17. Lakkaraju A, Finnemann SC, Rodriguez-Boulan E. The lipofuscin fluorophore A2E perturbs cholesterol metabolism in retinal pigment epithelial cells. Proc Natl Acad Sci U S A. 2007;104:11026-11031.
18. Sparrow JR, Cai B, Jang YP, Zhou J, Nakanishi K. A2E, a fluorophore of RPE lipofuscin, can destabilize membrane. Adv Exp Med Biol. 2006;572:63-68.
19. Schutt F, Davies S, Kopitz J, Holz FG, Boulton ME. Photodamage to human RPE cells by A2-E, a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci. 2000;41:2303-2308.
20. Sparrow JR, Nakanishi K, Parish CA. The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells. Invest Ophthalmol Vis Sci. 2000; 41:1981-1989.
21. Gutierrez DB, Blakeley L, Goletz PW, et al. Mass spectrometry provides accurate and sensitive quantitation of A2E. Photochem Photobiol Sci. 2010;9:1513-1519.
22. Maeda A, Golczak M, Maeda T, Palczewski K. Limited roles of Rdh8, Rdh12, and Abca4 in all-trans-retinal clearance in mouse retina. Invest Ophthalmol Vis Sci. 2009;50:5435-5443.
23. Pawlak A, Wrona M, Rozanowska M, et al. Comparison of the aerobic photoreactivity of A2E with its precursor retinal. Photochem Photobiol. 2003;77:253-258.
24. Maeda A, Golczak M, Chen Y, et al. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat Chem Biol. 2011;8:170-178.
25. Grey AC, Crouch RK, Koutalos Y, Schey KL, Ablonczy Z. Spatial localization of A2E in the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2011;52:3926-3933.
26. Bhosale P, Serban B, Bernstein PS. Retinal carotenoids can attenuate formation of A2E in the retinal pigment epithelium. Arch Biochem Biophys. 2009;483:175-181.
27. Parish CA, Hashimoto M, Nakanishi K, Dillon J, Sparrow J. Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc Natl Acad Sci U S A. 1998;95:14609-14613.
28. Sladkova K, Houska J, Havel J. Laser desorption ionization of red phosphorus clusters and their use for mass calibration in time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2009;23:3114-3118.
29. Haralampus-Grynaviski NM, Lamb LE, Clancy CM, et al. Spectroscopic and morphological studies of human retinal lipofuscin granules. Proc Natl Acad Sci U S A. 2003;100:3179-3184.
30. Del Priore LV, Kuo YH, Tezel TH. Age-related changes in human RPE cell density and apoptosis proportion in situ. Invest Ophthalmol Vis Sci. 2002;43:3312-3318.
31. Harman AM, Fleming PA, Hoskins RV, Moore SR. Development and aging of cell topography in the human retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1997;38:2016-2026.
32. Panda-Jonas S, Jonas JB, Jakobczyk-Zmija M. Retinal pigment epithelial cell count, distribution, and correlations in normal human eyes. Am J Ophthalmol. 1996;121:181-189.
33. Curcio CA, Messinger JD, Sloan KR, Mitra A, McGwin G, Spaide RF. Human chorioretinal layer thicknesses measured in macula-wide, high-resolution histologic sections. Invest Ophthalmol Vis Sci. 2011;52:3943-3954.
34. Wielgus AR, Collier RJ, Martin E, et al. Blue light induced A2E oxidation in rat eyes-experimental animal model of dry AMD. Photochem Photobiol Sci. 2010;9:1505-1512.
35. Ben-Shabat S, Itagaki Y, Jockusch S, Sparrow JR, Turro NJ, Nakanishi K. Formation of a nonaoxirane from A2E, a lipofuscin fluorophore related to macular degeneration, and evidence of singlet oxygen involvement. Angew Chem Int Engl. 2002;41:814-817.
36. Delori FC, Goger DG, Dorey CK. Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects. Invest Ophthalmol Vis Sci. 2001;42:1855-1866.