Spatial distribution of the pathways of cholesterol homeostasis in human retina

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Zheng, Wenchao ^a   Reem, Rachel E ^a   Omarova, Saida ^a   Huang, Suber ^a,b   DiPatre, Pier Luigi ^c   Charvet, Casey D ^a   Curcio, Christine A ^d   Pikuleva, Irina A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; COMPLEMENTARY DNA; FILIPIN; LIVER X RECEPTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ARTICLE; CATABOLISM; CHOLESTEROL HOMEOSTASIS; CHOLESTEROL SYNTHESIS; CHOROID; CONTROLLED STUDY; DNA SYNTHESIS; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RETINA; RNA ISOLATION;

CHOLESTEROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOMEOSTASIS; HUMANS; RETINA;

EID: 84861313738     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037926     Document Type: Article

References (75)

1. Yeagle PL, (1985) Cholesterol and the cell membrane. Biochim Biophys Acta 822: 267-287.
2. Brown MS, Goldstein JL, (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232: 34-47.
3. Dietschy JM, Turley SD, Spady DK, (1993) Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J Lipid Res 34: 1637-1659.
4. Russell DW, (2000) Oxysterol biosynthetic enzymes. Biochim Biophys Acta 1529: 126-135.
5. Brown MS, Goldstein JL, (2009) Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL. J Lipid Res 50 Suppl pp. S15-27.
6. Russell DW, (2008) 50 years of advances in bile acid synthesis and metabolism. J Lipid Res pp. S120-125.
7. Repa JJ, Mangelsdorf DJ, (2000) The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol 16: 459-481.
8. Dietschy JM, Turley SD, (2004) Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45: 1375-1397.
9. Horton JD, Goldstein JL, Brown MS, (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109: 1125-1131.
10. Russell DW, (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72: 137-174.
11. Kalaany NY, Mangelsdorf DJ, (2006) LXRS and FXR: the yin and yang of cholesterol and fat metabolism. Annu Rev Physiol 68: 159-191.
12. Zelcer N, Hong C, Boyadjian R, Tontonoz P, (2009) LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science 325: 100-104.
13. Fliesler SJ, Bretillon L, (2010) The ins and outs of cholesterol in the vertebrate retina. J Lipid Res 51: 3399-3413.
14. Tserentsoodol N, Sztein J, Campos M, Gordiyenko NV, Fariss RN, et al. (2006) Uptake of cholesterol by the retina occurs primarily via a low density lipoprotein receptor-mediated process. Mol Vis 12: 1306-1318.
15. Elner VM, (2002) Retinal pigment epithelial acid lipase activity and lipoprotein receptors: effects of dietary omega-3 fatty acids. Trans Am Ophthalmol Soc 100: 301-338.
16. Tserentsoodol N, Gordiyenko NV, Pascual I, Lee JW, Fliesler SJ, et al. (2006) Intraretinal lipid transport is dependent on high density lipoprotein-like particles and class B scavenger receptors. Mol Vis 12: 1319-1333.
17. Chen W, Stambolian D, Edwards AO, Branham KE, Othman M, et al. (2010) Genetic variants near TIMP3 and high-density lipoprotein-associated loci influence susceptibility to age-related macular degeneration. Proc Natl Acad Sci U S A 107: 7401-7406.
18. Neale BM, Fagerness J, Reynolds R, Sobrin L, Parker M, et al. (2010) Genome-wide association study of advanced age-related macular degeneration identifies a role of the hepatic lipase gene (LIPC). Proc Natl Acad Sci U S A 107: 7395-7400.
19. Reynolds R, Rosner B, Seddon JM, (2010) Serum lipid biomarkers and hepatic lipase gene associations with age-related macular degeneration. Ophthalmology 117: 1989-1995.
20. Mast N, Reem R, Bederman I, Huang S, DiPatre PL, et al. (2011) Cholestenoic acid is an important elimination product of cholesterol in the retina: comparison of retinal cholesterol metabolism to that in the brain. Invest Ophthalmol Vis Sci 52: 594-603.
21. Curcio CA, Johnson M, Huang JD, Rudolf M, (2010) Apolipoprotein B-containing lipoproteins in retinal aging and age-related macular degeneration. J Lipid Res 51: 451-467.
22. Curcio CA, Millican CL, Bailey T, Kruth HS, (2001) Accumulation of cholesterol with age in human Bruch's membrane. Invest Ophthalmol Vis Sci 42: 265-274.
23. Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, et al. (1997) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet 15: 236-246.
24. Kiser PD, Palczewski K, (2010) Membrane-binding and enzymatic properties of RPE65. Prog Retin Eye Res 29: 428-442.
25. Schnell SA, Staines WA, Wessendorf MW, (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47: 719-730.
26. Rudolf M, Curcio CA, (2009) Esterified cholesterol is highly localized to Bruch's membrane, as revealed by lipid histochemistry in wholemounts of human choroid. J Histochem Cytochem 57: 731-739.
27. Curcio CA, Rudolf M, Wang L, (2009) Histochemistry and lipid profiling combine for insights into aging and age-related maculopathy. Methods Mol Biol 580: 267-281.
28. Tserentsoodol N, Gordiyenko NV, Pascual I, Lee JW, Fliesler SJ, et al. (2006) Intraretinal lipid transport is dependent on high density lipoprotein-like particles and class B scavenger receptors. Mol Vis 12: 1319-1333.
29. Hayes KC, Lindsey S, Stephan ZF, Brecker D, (1989) Retinal pigment epithelium possesses both LDL and scavenger receptor activity. Invest Ophthalmol Vis Sci 30: 225-232.
30. Duncan KG, Bailey KR, Kane JP, Schwartz DM, (2002) Human retinal pigment epithelial cells express scavenger receptors BI and BII. Biochem Biophys Res Commun 292: 1017-1022.
31. Liao W-L, heo GY, Dodder N, Reem R, Mast N, et al. (2010) Quantification of Cholesterol-Metabolizing P450s CYP27A1 and CYP46A1 in Neural Tissues Reveals a Lack of Enzyme-Product Correlations in Human Retina but not Human Brain. J Proteome Res (conditional acceptance).
32. Dwyer MA, Kazmin D, Hu P, McDonnell DP, Malek G, (2011) Research resource: nuclear receptor atlas of human retinal pigment epithelial cells: potential relevance to age-related macular degeneration. Mol Endocrinol 25: 360-372.
33. Curcio CA, Sloan KR, Kalina RE, Hendrickson AE, (1990) Human photoreceptor topography. J Comp Neurol 292: 497-523.
34. Goldstein JL, Brown MS, (2009) The LDL receptor. Arterioscler Thromb Vasc Biol 29: 431-438.
35. Repa JJ, Mangelsdorf DJ, (2002) The liver X receptor gene team: potential new players in atherosclerosis. Nat Med 8: 1243-1248.
36. Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, et al. (2010) MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc Natl Acad Sci U S A 107: 17321-17326.
37. Marquart TJ, Allen RM, Ory DS, Baldan A, (2010) miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci U S A 107: 12228-12232.
38. Duncan KG, Hosseini K, Bailey KR, Yang H, Lowe RJ, et al. (2009) Expression of reverse cholesterol transport proteins ATP-binding cassette A1 (ABCA1) and scavenger receptor BI (SR-BI) in the retina and retinal pigment epithelium. Br J Ophthalmol 93: 1116-1120.
39. Claudepierre T, Paques M, Simonutti M, Buard I, Sahel J, et al. (2010) Lack of Niemann-Pick type C1 induces age-related degeneration in the mouse retina. Mol Cell Neurosci 43: 164-176.
40. Janowski BA, Grogan MJ, Jones SA, Wisely GB, Kliewer SA, et al. (1999) Structural requirements of ligands for the oxysterol liver X receptors LXRalpha and LXRbeta. Proc Natl Acad Sci U S A 96: 266-271.
41. Pikuleva IA, (2006) Cholesterol-metabolizing cytochromes P450. Drug Metab Dispos 34: 513-520.
42. Lee JW, Fuda H, Javitt NB, Strott CA, Rodriguez IR, (2006) Expression and localization of sterol 27-hydroxylase (CYP27A1) in monkey retina. Exp Eye Res 83: 465-469.
43. Ramirez DM, Andersson S, Russell DW, (2008) Neuronal expression and subcellular localization of cholesterol 24-hydroxylase in the mouse brain. J Comp Neurol 507: 1676-1693.
44. Bretillon L, Diczfalusy U, Bjorkhem I, Maire MA, Martine L, et al. (2007) Cholesterol-24S-hydroxylase (CYP46A1) is specifically expressed in neurons of the neural retina. Curr Eye Res 32: 361-366.
45. Guarneri P, Guarneri R, Cascio C, Pavasant P, Piccoli F, et al. (1994) Neurosteroidogenesis in rat retinas. J Neurochem 63: 86-96.
46. Jaliffa CO, Howard S, Hoijman E, Salido E, Sarmiento MI, et al. (2005) Effect of neurosteroids on the retinal gabaergic system and electroretinographic activity in the golden hamster. J Neurochem 94: 1666-1675.
47. Castanho MA, Coutinho A, Prieto MJ, (1992) Absorption and fluorescence spectra of polyene antibiotics in the presence of cholesterol. J Biol Chem 267: 204-209.
48. Fliesler SJ, Schroepfer GJ Jr, (1982) Sterol composition of bovine retinal rod outer segment membranes and whole retinas. Biochim Biophys Acta 711: 138-148.
49. Fliesler SJ, Anderson RE, (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22: 79-131.
50. Curcio CA, Presley JB, Malek G, Medeiros NE, Avery DV, et al. (2005) Esterified and unesterified cholesterol in drusen and basal deposits of eyes with age-related maculopathy. Exp Eye Res 81: 731-741.
51. Bretillon L, Acar N, Seeliger MW, Santos M, Maire MA, et al. (2008) ApoB100, LDLR-/- mice exhibit reduced electroretinographic response and cholesteryl esters deposits in the retina. Invest Ophthalmol Vis Sci 49: 1307-1314.
52. Boesze-Battaglia K, Hennessey T, Albert AD, (1989) Cholesterol heterogeneity in bovine rod outer segment disk membranes. J Biol Chem 264: 8151-8155.
53. Boesze-Battaglia K, Albert AD, (1990) Cholesterol modulation of photoreceptor function in bovine retinal rod outer segments. J Biol Chem 265: 20727-20730.
54. Bretillon L, Thuret G, Gregoire S, Acar N, Joffre C, et al. (2008) Lipid and fatty acid profile of the retina, retinal pigment epithelium/choroid, and the lacrimal gland, and associations with adipose tissue fatty acids in human subjects. Exp Eye Res 87: 521-528.
55. Harris RB, (1997) Appropriate animal models for clinical studies. Ann N Y Acad Sci 819: 155-168.
56. Liao WL, Heo GY, Dodder NG, Reem RE, Mast N, et al. (2011) Quantification of cholesterol-metabolizing P450s CYP27A1 and CYP46A1 in neural tissues reveals a lack of enzyme-product correlations in human retina but not human brain. J Proteome Res 10: 241-248.
57. Heo GY, Bederman I, Mast N, Liao WL, Turko IV, et al. (2011) Conversion of 7-ketocholesterol to oxysterol metabolites by recombinant CYP27A1 and retinal pigment epithelial cells. J Lipid Res 52: 1117-1127.
58. Fliesler SJ, Florman R, Rapp LM, Pittler SJ, Keller RK, (1993) In vivo biosynthesis of cholesterol in the rat retina. FEBS Lett 335: 234-238.
59. Fliesler SJ, Keller RK, (1997) Isoprenoid metabolism in the vertebrate retina. Int J Biochem Cell Biol 29: 877-894.
60. Curcio CA, Johnson M, Huang JD, Rudolf M, (2009) Aging, age-related macular degeneration, and the response-to-retention of apolipoprotein B-containing lipoproteins. Prog Retin Eye Res 28: 393-422.
61. Bonilha VL, Marmorstein AD, Cohen-Gould L, Rodriguez-Boulan E, (1997) Apical sorting of influenza hemagglutinin by transcytosis in retinal pigment epithelium. J Cell Sci 110 (Pt 15): 1717-1727.
62. Bojanic DD, Tarr PT, Gale GD, Smith DJ, Bok D, et al. (2010) Differential expression and function of ABCG1 and ABCG4 during development and aging. J Lipid Res 51: 169-181.
63. Phillips SE, Woodruff EA, 3rd, Liang P, Patten M, Broadie K, (2008) Neuronal loss of Drosophila NPC1a causes cholesterol aggregation and age-progressive neurodegeneration. J Neurosci 28: 6569-6582.
64. Albert AD, Boesze-Battaglia K, (2005) The role of cholesterol in rod outer segment membranes. Prog Lipid Res 44: 99-124.
65. Ohashi R, Mu H, Wang X, Yao Q, Chen C, (2005) Reverse cholesterol transport and cholesterol efflux in atherosclerosis. QJM 98: 845-856.
66. Cavelier C, Lorenzi I, Rohrer L, von Eckardstein A, (2006) Lipid efflux by the ATP-binding cassette transporters ABCA1 and ABCG1. Biochim Biophys Acta 1761: 655-666.
67. Williams DL, Connelly MA, Temel RE, Swarnakar S, Phillips MC, et al. (1999) Scavenger receptor BI and cholesterol trafficking. Curr Opin Lipidol 10: 329-339.
68. de La Llera-Moya M, Connelly MA, Drazul D, Klein SM, Favari E, et al. (2001) Scavenger receptor class B type I affects cholesterol homeostasis by magnifying cholesterol flux between cells and HDL. J Lipid Res 42: 1969-1978.
69. DeBose-Boyd RA, (2008) Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase. Cell Res 18: 609-621.
70. Pfrieger FW, (2003) Cholesterol homeostasis and function in neurons of the central nervous system. Cell Mol Life Sci 60: 1158-1171.
71. Omkumar RV, Darnay BG, Rodwell VW, (1994) Modulation of Syrian hamster 3-hydroxy-3-methylglutaryl-CoA reductase activity by phosphorylation. Role of serine 871. J Biol Chem 269: 6810-6814.
72. Gordiyenko N, Campos M, Lee JW, Fariss RN, Sztein J, et al. (2004) RPE cells internalize low-density lipoprotein (LDL) and oxidized LDL (oxLDL) in large quantities in vitro and in vivo. Invest Ophthalmol Vis Sci 45: 2822-2829.
73. Meaney S, Bodin K, Diczfalusy U, Bjorkhem I, (2002) On the rate of translocation in vitro and kinetics in vivo of the major oxysterols in human circulation: critical importance of the position of the oxygen function. J Lipid Res 43: 2130-2135.
74. Babiker A, Andersson O, Lund E, Xiu RJ, Deeb S, et al. (1997) Elimination of cholesterol in macrophages and endothelial cells by the sterol 27-hydroxylase mechanism. Comparison with high density lipoprotein-mediated reverse cholesterol transport. J Biol Chem 272: 26253-26261.
75. Dotti MT, Rufa A, Federico A, (2001) Cerebrotendinous xanthomatosis: heterogeneity of clinical phenotype with evidence of previously undescribed ophthalmological findings. J Inherit Metab Dis 24: 696-706.