Beta cyclodextrins bind, stabilize, and remove lipofuscin bisretinoids from retinal pigment epithelium

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 14, 2014, Pages

  Nociari, Marcelo M ^a   Lehmann, Guillermo L ^a   Perez Bay, Andres E ^a   Radu, Roxana A ^b   Jiang, Zhichun ^b   Goicochea, Shelby ^a   Schreiner, Ryan ^a   Warren, J David ^a   Shan, Jufang ^a   De Beaumais, Ségolène Adam ^c   Ménand, Mickaël ^c   Sollogoub, Matthieu ^c   Maxfield, Frederick R ^a   Rodriguez Boulan, Enrique ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b JULES STEIN EYE INSTITUTE   (United States)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Aging; Lipofuscinosis; Residual bodies; Retinopathy

Indexed keywords

BETA CYCLODEXTRIN DERIVATIVE; LIPOFUSCIN; RETINOID;

ABSORPTION SPECTROSCOPY; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLINDNESS; COMPUTER MODEL; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUSEN; ENCAPSULATION; EX VIVO STUDY; FLUORESCENCE MICROSCOPY; FLUORESCENCE SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROPHOBICITY; IMMUNOFLUORESCENCE; LYSOSOME; MOLECULAR MODEL; MOLECULE; MOUSE; NONHUMAN; OXIDATION; PHOTOOXIDATION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA NEUROEPITHELIAL LAYER; SOLUBILITY;

AGING; LIPOFUSCINOSIS; RESIDUAL BODIES; RETINOPATHY;

ANIMALS; BETA-CYCLODEXTRINS; BINDING SITES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTER SIMULATION; FLUORESCENCE; LIPOFUSCIN; MICE; MICE, KNOCKOUT; OXIDATION-REDUCTION; RETINAL PIGMENT EPITHELIUM; RETINOIDS;

EID: 84898047300     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400530111     Document Type: Article

References (56)

1. Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85(3): 845-881.
2. Sparrow JR, Hicks D, Hamel CP (2010) The retinal pigment epithelium in health and disease. Curr Mol Med 10(9):802-823.
3. Sparrow JR, Boulton M (2005) RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 80(5):595-606.
4. Eldred GE, Lasky MR (1993) Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 361(6414):724-726.
5. Ng K-P, et al. (2008) Retinal pigment epithelium lipofuscin proteomics. Mol Cell Proteomics 7(7):1397-1405.
6. Maeda A, Maeda T, Golczak M, Palczewski K (2008) Retinopathy in mice induced by disrupted all-trans-retinal clearance. J Biol Chem 283(39):26684-26693.
7. Weng J, et al. (1999) Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell 98(1): 13-23.
8. Wu Y, Zhou J, Fishkin N, Rittmann BE, Sparrow JR (2011) Enzymatic degradation of A2E, a retinal pigment epithelial lipofuscin bisretinoid. J Am Chem Soc 133(4): 849-857.
9. Sparrow JR, Kim SR, Cuervo AM, Bandhyopadhyayand U (2008) A2E, a pigment of RPE lipofuscin, is generated from the precursor, A2PE by a lysosomal enzyme activity. Adv Exp Med Biol 613:393-398.
10. Schütt F, Davies S, Kopitz J, Holz FG, Boulton ME (2000) Photodamage to human RPE cells by A2-E, a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 41(8): 2303-2308.
11. Sparrow JR, Cai B (2001) Blue light-induced apoptosis of A2E-containing RPE: Involvement of caspase-3 and protection by Bcl-2. Invest Ophthalmol Vis Sci 42(6): 1356-1362.
12. Holz FG, Bellman C, Staudt S, Schütt F, Völcker HE (2001) Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration. Invest Ophthalmol Vis Sci 42(5):1051-1056.
13. Allikmets R, et al. (1997) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet 15(3):236-246.
14. Washington I, Jockusch S, Itagaki Y, Turro NJ, Nakanishi K (2005) Superoxidation of bisretinoids. Angew Chem Int Ed Engl 44(43):7097-7100.
15. Kim SR, Jockusch S, Itagaki Y, Turro NJ, Sparrow JR (2008) Mechanisms involved in A2E oxidation. Exp Eye Res 86(6):975-982.
16. Jang YP, Matsuda H, Itagaki Y, Nakanishi K, Sparrow JR (2005) Characterization of peroxy-A2E and furan-A2E photooxidation products and detection in human and mouse retinal pigment epithelial cell lipofuscin. J Biol Chem 280(48):39732-39739.
17. Sparrow JR, Parish CA, Hashimoto M, Nakanishi K (1999) A2E, a lipofuscin fluorophore, in human retinal pigmented epithelial cells in culture. Invest Ophthalmol Vis Sci 40(12):2988-2995.
18. Ragauskaite L, Heckathorn RC, Gaillard ER (2001) Environmental effects on the photochemistry of A2-E, a component of human retinal lipofuscin. Photochem Photobiol 74(3):483-488.
19. De S, Sakmar TP (2002) Interaction of A2E with model membranes. Implications to the pathogenesis of age-related macular degeneration. J Gen Physiol 120(2):147-157.
20. Abi-Mosleh L, Infante RE, Radhakrishnan A, Goldstein JL, Brown MS (2009) Cyclodextrin overcomes deficient lysosome-to-endoplasmic reticulum transport of cholesterol in Niemann-Pick type C cells. Proc Natl Acad Sci USA 106(46):19316-19321.
21. Rosenbaum AI, Maxfield FR (2011) Niemann-Pick type C disease: Molecular mechanisms and potential therapeutic approaches. J Neurochem 116(5):789-795.
22. Ben-Shabat S, et al. (2002) Formation of a nonaoxirane from A2E, a lipofuscin fluorophore related to macular degeneration, and evidence of singlet oxygen involvement. Angew Chem Int Ed Engl 41(5):814-817.
23. Wang Z, Keller LMM, Dillon J, Gaillard ER (2006) Oxidation of A2E results in the formation of highly reactive aldehydes and ketones. Photochem Photobiol 82(5): 1251-1257.
24. Schurig HPNV (1990) Neue analytische Methoden: Gaschromatographische Enantiomerentrennung an Cyclodextrinderivaten (Gas chromatographic Separation of Enantiomers on Cyclodextrin Derivatives). Angew Chem Int Ed Engl 29:939-1076.
25. Benesi HA, Hildebrand JH (1949) A Spectrophotometric Investigation of the Interaction of Iodine with Aromatic Hydrocarbons. J Am Chem Soc 71:2703-2707.
26. Baker GA, Crane NJ, Mayrhofer RC, Betts TA (2002) Cyclodextrin Inclusion Complexes with a Solvatochromic Fluorescent Probe. J Chem Educ 79:1261.
27. Breslow R, Halfon S, Zhang B (1995) Molecular recognition by cyclodextrin dimers. Tetrahedron 51:377-388.
28. Rosenbaum AI, Zhang G, Warren JD, Maxfield FR (2010) Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc Natl Acad Sci USA 107(12):5477-5482.
29. Mondal M, Mesmin B, Mukherjee S, Maxfield FR (2009) Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol Biol Cell 20(2):581-588.
30. Sparrow JR, Kim SR, Wu Y (2010) Experimental approaches to the study of A2E, a bisretinoid lipofuscin chromophore of retinal pigment epithelium. Methods Mol Biol 652:315-327.
31. Radu RA, et al. (2008) Accelerated accumulation of lipofuscin pigments in the RPE of a mouse model for Abca4-mediated retinal dystrophies following Vitamin A supplementation. Invest Ophthalmol Vis Sci 49(9):3821-3829.
32. Wielgus AR, Chignell CF, Ceger P, Roberts JE (2010) Comparison of A2E cytotoxicity and phototoxicity with all-trans-retinal in human retinal pigment epithelial cells. Photochem Photobiol 86(4):781-791.
33. Maeda A, et al. (2012) Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat Chem Biol 8(2):170-178.
34. Maeda A, et al. (2009) Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J Biol Chem 284(22):15173-15183.
35. Maeda T, Golczak M, Maeda A (2012) Retinal photodamage mediated by all-transretinal. Photochem Photobiol 88(6):1309-1319.
36. Godley BF, et al. (2005) Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem 280(22):21061-21066.
37. Sokolov VS, et al. (2007) Interaction of pyridinium bis-retinoid (A2E) with bilayer lipid membranes. J Photochem Photobiol B 86(2):177-185.
38. Baltazar GC, et al. (2012) Acidic nanoparticles are trafficked to lysosomes and restore an acidic lysosomal pH and degradative function to compromised ARPE-19 cells. PLoS ONE 7(12):e49635.
39. Holz FG, et al. (1999) Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 40(3):737-743.
40. Jarrett SG, BoultonME (2012) Consequences of oxidative stress in age-related macular degeneration. Mol Aspects Med 33(4):399-417.
41. Lakkaraju A, Finnemann SC, Rodriguez-Boulan E (2007) The lipofuscin fluorophore A2E perturbs cholesterol metabolism in retinal pigment epithelial cells. Proc Natl Acad Sci USA 104(26):11026-11031.
42. Zhou J, Kim SR, Westlund BS, Sparrow JR (2009) Complement activation by bisretinoid constituents of RPE lipofuscin. Invest Ophthalmol Vis Sci 50(3):1392-1399.
43. Ma W, Coon S, Zhao L, Fariss RN, Wong WT (2013) A2E accumulation influences retinal microglial activation and complement regulation. Neurobiol Aging 34(3): 943-960.
44. Anderson OA, Finkelstein A, Shima DT (2013) A2E induces IL-1β production in retinal pigment epithelial cells via the NLRP3 inflammasome. PLoS ONE 8(6):e67263.
45. Holtkamp GM, et al. (1998) Polarized secretion of IL-6 and IL-8 by human retinal pigment epithelial cells. Clin Exp Immunol 112(1):34-43.
46. Iriyama A, et al. (2009) A2E, a component of lipofuscin, is pro-angiogenic in vivo. J Cell Physiol 220(2):469-475.
47. Buschini E, Piras A, Nuzzi R, Vercelli A (2011) Age related macular degeneration and drusen: Neuroinflammation in the retina. Prog Neurobiol 95(1):14-25.
48. Kanda A, Abecasis G, Swaroop A (2008) Inflammation in the pathogenesis of agerelated macular degeneration. Br J Ophthalmol 92(4):448-450.
49. Girotti AW (1985) Mechanisms of lipid peroxidation. J Free Radic Biol Med 1(2):87-95.
50. Sparrow JR, et al. (2002) Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE. Invest Ophthalmol Vis Sci 43(4):1222-1227.
51. Yoon KD, Yamamoto K, Ueda K, Zhou J, Sparrow JR (2012) A novel source of methylglyoxal and glyoxal in retina: Implications for age-related macular degeneration. PLoS ONE 7(7):e41309.
52. Plazzo AP, et al. (2012) Uptake of a fluorescent methyl-β- cyclodextrin via clathrindependent endocytosis. Chem Phys Lipids 165(5):505-511.
53. Vance JE, Peake KB (2011) Function of the Niemann-Pick type C proteins and their bypass by cyclodextrin. Curr Opin Lipidol 22(3):204-209.
54. Davidson CD, et al. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE 4(9):e6951.
55. Yao J, et al. (2012) Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease. J Exp Med 209(13):2501-2513.
56. Nilsson E, Yin D (1997) Preparation of artificial ceroid/lipofuscin by UV-oxidation of subcellular organelles. Mech Ageing Dev 99(1):61-78.