Biological effects of native and oxidized low-density lipoproteins in cultured human retinal pigment epithelial cells

Experimental Eye Research

Volumn 88, Issue 3, 2009, Pages 495-503

  Yu, Alice L ^a   Lorenz, Reinhard L ^a   Haritoglou, Christos ^a   Kampik, Anselm ^a   Welge Lussen, Ulrich ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

age related macular degeneration; lipoprotein; retinal pigment epithelium

Indexed keywords

BETA GALACTOSIDASE; COLLAGEN TYPE 4; COLLAGEN TYPE 4 ALPHA 2; FIBRONECTIN; HIGH DENSITY LIPOPROTEIN; LAMININ; LAMININ ALPHA 1; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; OXIDIZED LOW DENSITY LIPOPROTEIN; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CELL LOSS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; HUMAN; PIGMENT CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENESCENCE;

ADULT; CELL AGING; CELL DEATH; CELLS, CULTURED; CHOLESTEROL, HDL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HUMANS; LIPOPROTEINS, LDL; MACULAR DEGENERATION; MIDDLE AGED; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA2;

EID: 61549098691     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2008.10.028     Document Type: Article

References (73)

1. Alge C.S., Priglinger S.G., Neubauer A.S., Kampik A., Zillig M., Bloemendal H., and Welge-Lussen U. Retinal pigment epithelium is protected against apoptosis by alphaB-crystallin. Invest. Ophthalmol. Vis. Sci. 43 (2002) 3575-3582
2. Al-Shaer M.H., Choueiri N.E., Correia M.L., Sinkey C.A., Barenz T.A., and Haynes W.G. Effects of aging and atherosclerosis on endothelial and vascular smooth muscle function in humans. Int. J. Cardiol. 109 (2006) 201-206
3. An E., Lu X., Flippin J., Devaney J.M., Halligan B., Hoffman E.P., Strunnikova N., Csaky K., and Hathout Y. Secreted proteome profiling in human RPE cell cultures derived from donors with age related macular degeneration and age matched healthy donors. J. Proteome Res. 5 (2006) 2599-2610
4. Bachem M.G., Wendelin D., Schneiderhan W., Haug C., Zorn U., Gross H.J., Schmid-Kotsas A., and Grünert A. Depending on their concentration oxidized low density lipoproteins stimulate extracellular matrix synthesis or induce apoptosis in human coronary artery smooth muscle cells. Clin. Chem. Lab. Med. 37 (1999) 319-326
5. Boullier A., Bird D.A., Chang M.K., Dennis E.A., Friedman P., Gillotre-Taylor K., Hörkkö S., Palinski W., Quehenberger O., Shaw P., Steinberg D., Terpstra V., and Witztum J.L. Scavenger receptors, oxidized LDL and atherosclerosis. Ann. N. Y. Acad. Sci. 947 (2001) 214-222
6. Campochiaro P.A., Jerdon J.A., and Glaser B.M. The extracellular matrix of human retinal pigment epithelial cells in vivo and its synthesis in vitro. Invest. Ophthalmol. Vis. Sci. 27 (1986) 1615-1621
7. Chamberlain M., Baird P., Dirani M., and Guymer R. Unraveling a complex genetic disease: age-related macular degeneration. Surv. Ophthalmol. 51 (2006) 576-586
8. Cipollone F., Fazia M., Mincione G., Iezzi A., Pini B., Cuccurullo C., Ucchino S., Spigonardo F., Di Nisio M., Cuccurullo F., Mezzetti A., and Porreca E. Increased expression of transforming growth factor-beta1 as a stabilizing factor in human atherosclerotic plaques. Stroke 35 (2004) 2253-2257
9. DeWan A., Bracken M.B., and Hoh J. Two genetic pathways for age-related macular degeneration. Curr. Opin. Genet. Dev. 17 (2007) 228-233
10. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9363-9367
11. Ding G., van Goor H., Ricardo S.D., Orlowski J.M., and Diamond J.R. Oxidized LDL stimulates the expression of TGF-beta and fibronectin in human glomerular epithelial cells. Kidney Int. 51 (1997) 147-154
12. Edwards A.O., and Malek G. Molecular genetics of AMD and current animal models. Angiogenesis 10 (2007) 119-132
13. Feher J., Kovacs I., Artico M., Cavallotti C., Papale A., and Balacco Gabrieli C. Mitochondrial alterations of retinal pigment epithelium in age-related macular degeneration. Neurobiol. Aging 27 (2006) 983-993
14. Fliesler S.J., Florman R., Rapp L.M., Pittler S.J., and Keller R.K. In vivo biosynthesis of cholesterol in the rat retina. FEBS Lett. 335 (1993) 234-238
15. Fukuchi M., Watanabe J., Kumagai K., Baba S., Shinozaki T., Miura M., Kagaya Y., and Shirato K. Normal and oxidized low density lipoproteins accumulate deep in physiologically thickened intima of human coronary arteries. Lab. Invest. 82 (2002) 1437-1447
16. 2. Exp. Eye Res. 74 (2002) 663-669
17. Gordiyenko N., Campos M., Lee J.W., Fariss R.N., Sztein J., and Rodriguez I.R. RPE cells internalize low-density lipoprotein (LDL) and oxidized LDL (oxLDL) in large quantities in vitro and in vivo. Invest. Ophthalmol. Vis. Sci. 45 (2004) 2822-2829
18. Guymer R.H., Chiu A.W., Lim L., and Baird P.N. HMG CoA reductase inhibitors (statins): do they have a role in age-related macular degeneration?. Surv. Ophthalmol. 50 (2005) 194-206
19. Hardwick S.J., Hegyi L., Clare K., Law N.S., Carpenter K.L., Mitchinson M.J., and Skepper J.N. Apoptosis in human monocyte-macrophages exposed to oxidized low density lipoprotein. J. Pathol. 179 (1996) 294-302
20. Hawkins B.S., Bird A., Klein R., and West S.K. Epidemiology of age-related macular degeneration. Mol. Vis. 5 (1999) 26
21. Holz F.G., Sheraidah G., Pauleikhoff D., and Bird A.C. Analysis of lipid deposits extracted from human macular and peripheral Bruch's membrane. Arch. Ophthalmol. 112 (1994) 402-406
22. Honda S., Hjelmeland L.M., and Handa J.T. Senescence associated beta galactosidase activity in human retinal pigment epithelial cells exposed to mild hyperoxia in vitro. Br. J. Ophthalmol. 86 (2002) 159-162
23. Hoppe G., O'Neil J., Hoff H.F., and Sears J. Accumulation of oxidized lipid-protein complexes alters phagosome maturation in retinal pigment epithelium. Cell Mol. Life Sci. 61 (2004) 1664-1674
24. Hyman L., and Neborsky R. Risk factors for age-related macular degeneration: an update. Curr. Opin. Ophthalmol. 13 (2002) 171-175
25. Imanishi T., Hano T., Sawamura T., and Nishio I. Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin. Exp. Pharmacol. Physiol. 31 (2004) 407-413
26. Kamei M., Yoneda K., Kume N., Suzuki M., Itabe H., Matsuda K., Shimaoka T., Minami M., Yonehara S., Kita T., and Kinoshita S. Scavenger receptors for oxidized lipoprotein in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 48 (2007) 1801-1807
27. Klein R., Klein B.E., and Linton K.L.P. Prevalence of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology 99 (1992) 933-943
28. Klein R., Klein B.E., Tomany S.C., and Cruickshanks K.J. The association of cardiovascular disease with the long-term incidence of age-related maculopathy: the Beaver Dam Eye study. Ophthalmology 110 (2003) 636-643
29. Klein R., Peto T., Bird A., and Vannewkirk M.R. The epidemiology of age-related macular degeneration. Am. J. Ophthalmol. 137 (2004) 486-495
30. Kliffen M., Sharma H.S., Mooy C.M., Kerkvliet S., and de Jong P.T. Increased expression of angiogenic growth factors in age-related maculopathy. Br. J. Ophthalmol. 81 (1997) 154-162
31. Lee H.S. Oxidized LDL, glomerular mesangial cells and collagen. Diabetes Res. Clin. Pract. 45 (1999) 117-122
32. van Leeuwen R., Klaver C.C., Vingerling J.R., Hofman A., and de Jong P.T. Epidemiology of age-related maculopathy: a review. Eur. J. Epidemiol. 18 (2003) 845-854
33. Leschey K.H., Hackett S.F., Singer J.H., and Campochiaro P.A. Growth factor responsiveness of human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 31 (1990) 839-846
34. Li D., Yang B., and Mehta J.L. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am. J. Physiol. 275 (1998) 568-576
35. Maier J.A., Barenghi L., Bradamante S., and Pagani F. Induction of human endothelial cell growth by mildly oxidized low density lipoprotein. Atherosclerosis 123 (1996) 115-121
36. Malek G., Li C.M., Guidry C., Medeiros N.E., and Curcio C.A. Apolipoprotein B in cholesterol-containing drusen and basal deposits of human eyes with age-related maculopathy. Am. J. Pathol. 162 (2003) 413-425
37. Mares-Perlman J.A., Brady W.E., Klein R., VandenLangenberg G.M., Klein B.E., and Palta M. Dietary fat and age-related maculopathy. Arch. Ophthalmol. 113 (1995) 743-748
38. Minamino T., Miyauchi H., Yoshida T., Tateno K., and Komuro I. The role of vascular cell senescence in atherosclerosis: antisenescence as a novel therapeutic strategy for vascular aging. Curr. Vasc. Pharmacol. 2 (2004) 141-148
39. Minamino T., and Komuro I. Vascular cell senescence: contribution to atherosclerosis. Circ. Res. 100 (2007) 15-26
40. Mitchell P., Wang J.J., Smith W., and Leeder S.R. Smoking and the 5-year incidence of age-related maculopathy: the Blue Mountains Eye study. Arch. Ophthalmol. 120 (2002) 1357-1363
41. Nakajima K., Nakano T., and Tanaka A. The oxidative modification hypothesis of atherosclerosis: the comparison of atherogenic effects on oxidized LDL and remnant lipoproteins in plasma. Clin. Chim. Acta 367 (2006) 36-47
42. Newby A.C. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol. Rev. 85 (2005) 1-31
43. Nilsson S.E., Sundelin S.P., Wihlmark U., and Brunk U.T. Aging of cultured retinal pigment epithelial cells: oxidative reactions, lipofuscin formation and blue light damage. Doc. Ophthalmol. 106 (2003) 13-16
44. Petrukhin K. New therapeutic targets in atrophic age-related macular degeneration. Expert Opin. Ther. Targets 11 (2007) 625-639
45. Rahaman S.O., Lennon D.J., Febbraio M., Podrez E.A., Hazen S.L., and Silverstein R.L. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 4 (2006) 211-221
46. Robman L., McNeil J., Dimitrov P., Dowrick A., Tikellis G., Nicolas C., Cameron J., Guymer R., McGrath B., and McCarty C. Methodology of the Cardiovascular Health and Age-Related Maculopathy (CHARM) Study. Ophthalmic Epidemiol. 11 (2004) 161-179
47. Rodriguez I.R., Alam S., and Lee J.W. Cytotoxicity of oxidized low-density lipoprotein in cultured RPE cells is dependent on the formation of 7-ketocholesterol. Invest. Ophthalmol. Vis. Sci. 45 (2004) 2830-2837
48. Roh D.D., Kamanna V.S., and Kirschenbaum M.A. Oxidative modification of low-density lipoprotein enhances mesangial cell protein synthesis and gene expression of extracellular matrix proteins. Am. J. Nephrol. 18 (1998) 344-350
49. Roth F., Bindewald A., and Holz F.G. Keypathophysiologic pathways in age-related macular disease. Graefe's Arch. Clin. Exp. Ophthalmol. 242 (2004) 710-716
50. Ruberti J.W., Curcio C.A., Millican C.L., Bailey T., and Kruth H.S. Accumulation of cholesterol with age in human Bruch's membrane. Invest. Ophthalmol. Vis. Sci. 42 (2001) 265-274
51. Rubic T., and Lorenz R.L. Downregulated CD36 and oxLDL uptake and stimulated ABCA1/G1 and cholesterol efflux as anti-atherosclerotic mechanisms of interleukin-10. Cardiovasc. Res. 69 (2006) 527-535
52. Ryeom S.W., Silverstein R.L., Scotto A., and Sparrow J.R. Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36. J. Biol. Chem. 271 (1996) 20536-20539
53. Sarangarajan R., and Apte S.P. Review melanization and phagocytosis: implications for age related macular degeneration. Mol. Vis. 11 (2005) 482-490
54. van der Schaft T.L., Mooy C.M., de Bruijn W.C., Bosman F.T., and de Jong P.T. Immunohistochemical light and electron microscopy of basal laminar deposit. Graefe's Arch. Clin. Exp. Ophthalmol. 232 (1994) 40-46
55. Schmidt S., Qin X., Schmidt M.A., Martin E.R., and Hauser E.R. Interpreting analyses of continuous covariates in affected sibling pair linkage studies. Genet. Epidemiol. 31 (2007) 541-552
56. Schneiderhan W., Schmid-Kotsas A., Zhao J., Grünert A., Nüssler A., Weidenbach H., Menke A., Schmid R.M., Adler G., and Bachem M.G. Oxidized low-density lipoproteins bind to the scavenger receptor, CD36, of hepatic stellate cells and stimulate extracellular matrix synthesis. Hepatology 34 (2001) 729-737
57. Schulz T., Schiffl H., Scheithe R., Hrboticky N., and Lorenz R. Preserved antioxidative defense of lipoproteins in renal failure and during hemodialysis. Am. J. Kidney Dis. 25 (1995) 564-571
58. Schwartz C.J., Valente A.J., Sprague E.A., Kelley J.L., and Nerem R.M. The pathogenesis of atherosclerosis: an overview. Clin. Cardiol. 14 (1991) 11-16
59. Shi Q., Hubbard G.B., Kushwaha R.S., Rainwater D., Thomas III C.A., Leland M.M., Vandeberg J.L., and Wang X.L. Endothelial senescence after high-cholesterol, high-fat diet challenge in baboons. Am. J. Physiol. Heart Circ. Physiol. 292 (2007) 2913-2920
60. Sivaprasad S., Bailey T.A., and Chong V.N. Bruch's membrane and the vascular intima: is there a common basis for age-related changes and disease?. Clin. Exp. Ophthalmol. 33 (2005) 518-523
61. Smith W., Assink J., Klein R., Mitchell P., Klaver C.C., Klein B.E., Hofman A., Jensen S., Wang J.J., and de Jong P.T. Risk factors for age-related macular degeneration: pooled findings from three continents. Ophthalmology 108 (2001) 697-704
62. Stoneman V.E., and Bennett M.R. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin. Sci. (Lond.) 107 (2004) 343-354
63. Takahashi Y., Zhu H., and Yoshimoto T. Essential roles of lipoxygenases in LDL oxidation and development of atherosclerosis. Antioxid. Redox Signal 7 (2005) 425-431
64. Tan J.S., Mitchell P., Smith W., and Wang J.J. Cardiovascular risk factors and the long-term incidence of age-related macular degeneration: the Blue Mountains Eye Study. Ophthalmology 114 (2007) 1143-1150
65. Thornton J., Edwards R., Mitchell P., Harrison R.A., Buchan I., and Kelly S.P. Smoking and age-related macular degeneration: a review of association. Eye 19 (2005) 935-944
66. Tsimikas S. Oxidized low-density lipoprotein biomarkers in atherosclerosis. Curr. Atheroscler. Rep. 8 (2006) 55-61
67. Vingerling J.R., Dielemans I., Hofman A., Grobbee D.E., Hijmering M., Kramer C.F., and de Jong P.T. The prevalence of age-related maculopathy in the Rotterdam Study. Ophthalmology 102 (1995) 205-210
68. Vingerling J.R., Dielemans I., Bots M.L., Hofman A., Grobbee D.E., and de Jong P.T.V.M. Age-related macular degeneration is associated with atherosclerosis: the Rotterdam Study. Am. J. Epidemiol. 142 (1995) 404-409
69. Weber C., Draude G., Weber K.S., Wubert J., Lorenz R.L., and Weber P.C. Downregulation by tumor necrosis factor-alpha of monocyte CCR2 expression and monocyte chemotactic protein-1-induced transendothelial migration is antagonized by oxidized low-density lipoprotein: a potential mechanism of monocyte retention in atherosclerotic lesions. Atherosclerosis 145 (1999) 115-123
70. Yesner L.M., Huh H.Y., Pearce S.F., and Silverstein R.L. Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. Arterioscler. Thromb. Vasc. Biol. 16 (1996) 1019-1025
71. Young R.W. Pathophysiology of age-related macular degeneration. Surv. Ophthalmol. 31 (1987) 291-306
72. Zarbin M.A. Current concepts in the pathogenesis of age-related macular degeneration. Arch. Ophthalmol. 122 (2004) 598-614
73. Zhu C., Ying D., Zhou D., Mi J., Zhang W., Chang Q., and Li L. Expression of TGF-beta1 in smooth muscle cells regulates endothelial progenitor cells migration and differentiation. J. Surg. Res. 125 (2005) 151-156