7-Dehydrocholesterol-derived oxysterols and retinal degeneration in a rat model of Smith-Lemli-Opitz syndrome

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 6, 2012, Pages 877-883

  Xu, Libin ^a   Sheflin, Lowell G ^b   Porter, Ned A ^a   Fliesler, Steven J ^b,c,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA WESTERN NEW YORK HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d SUNY EYE INSTITUTE   (United States)

Author keywords

7 dehydrocholesterol; 7 ketocholesterol; Oxidation; Oxysterol; Retinal degeneration; Smith Lemli Opitz Syndrome

Indexed keywords

1,4 BIS(2 CHLOROBENZYLAMINOMETHYL)CYCLOHEXANE; 7 DEHYDROCHOLESTEROL; 7 OXOCHOLESTEROL; ANTIOXIDANT; CHOLESTEROL; CYTOCHROME P450;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; OXIDATION; PEROXIDATION; PRIORITY JOURNAL; RAT; RETINA DEGENERATION; SMITH LEMLI OPITZ SYNDROME; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; CHOLESTEROL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DEHYDROCHOLESTEROLS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; KETOCHOLESTEROLS; MALE; MASS SPECTROMETRY; MOLECULAR STRUCTURE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL DEGENERATION; SMITH-LEMLI-OPITZ SYNDROME; TRANS-1,4-BIS(2-CHLOROBENZAMINOMETHYL)CYCLOHEXANE DIHYDROCHLORIDE;

MUS; RATTUS;

EID: 84859301170     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.03.001     Document Type: Article

References (58)

1. R.I. Kelley, and R.C. Hennekam The Smith-Lemli-Opitz syndrome J. Med. Genet. 37 2000 321 335 (Pubitemid 30261263)
2. F.D. Porter, and G.E. Herman Malformation syndromes caused by disorders of cholesterol synthesis J. Lipid Res. 52 2011 6 34
3. M. Fierro, A.J. Martinez, J.W. Harbison, and S.H. Hay Smith-Lemli-Opitz syndrome: neuropathological and ophthalmological observations Dev. Med. Child Neurol. 19 1977 57 62 (Pubitemid 8036543)
4. L.O. Atchaneeyasakul, L.M. Linck, W.E. Connor, R.G. Weleber, and R.D. Steiner Eye findings in 8 children and a spontaneously aborted fetus with RSH/Smith-Lemli-Opitz syndrome Am. J. Med. Genet. 80 1998 501 505 (Pubitemid 29002018)
5. E.R. Elias, R.M. Hansen, M. Irons, N.B. Quinn, and A.B. Fulton Rod photoreceptor responses in children with Smith-Lemli-Opitz syndrome Arch. Ophthalmol. 121 2003 1738 1743 (Pubitemid 37517441)
6. D. Haas, S.F. Garbade, C. Vohwinkel, N. Muschol, F.K. Trefz, J.M. Penzien, J. Zschocke, G.F. Hoffmann, and P. Burgard Effects of cholesterol and simvastatin treatment in patients with Smith-Lemli-Opitz syndrome (SLOS) J. Inherit. Metab. Dis. 30 2007 375 387 (Pubitemid 46881685)
7. M. Irons, E.R. Elias, D. Abuelo, M.J. Bull, C.L. Greene, V.P. Johnson, L. Keppen, C. Schanen, G.S. Tint, and G. Salen Treatment of Smith-Lemli-Opitz syndrome: results of a multicenter trial Am. J. Med. Genet. 68 1997 311 314 (Pubitemid 27081814)
8. D.M. Sikora, M. Ruggiero, K. Petit-Kekel, L.S. Merkens, W.E. Connor, and R.D. Steiner Cholesterol supplementation does not improve developmental progress in Smith-Lemli-Opitz syndrome J. Pediatr. 144 2004 783 791 (Pubitemid 38858097)
9. E. Tierney, S.K. Conley, H. Goodwin, and F.D. Porter Analysis of short-term behavioral effects of dietary cholesterol supplementation in Smith-Lemli-Opitz syndrome Am. J. Med. Genet. A 152A 2010 91 95
10. P.E. Jira, R.A. Wevers, J. de Jong, E. Rubio-Gozalbo, F.S. Janssen-Zijlstra, A.F. van Heyst, R.C. Sengers, and J.A. Smeitink Simvastatin. A new therapeutic approach for Smith-Lemli-Opitz syndrome J. Lipid Res. 41 2000 1339 1346 (Pubitemid 30666899)
11. L. Starck, A. Lovgren-Sandblom, and I. Bjorkhem Simvastatin treatment in the SLO syndrome: a safe approach? Am. J. Med. Genet. 113 2002 183 189 (Pubitemid 35231551)
12. Y.M. Chan, L.S. Merkens, W.E. Connor, J.B. Roullet, J.A. Penfield, J.M. Jordan, R.D. Steiner, and P.J. Jones Effects of dietary cholesterol and simvastatin on cholesterol synthesis in Smith-Lemli-Opitz syndrome Pediatr. Res. 65 2009 681 685
13. J.A. Farmer Pleiotropic effects of statins Curr. Atheroscler. Rep. 2 2000 208 217
14. L. Xu, T.A. Davis, and N.A. Porter Rate constants for peroxidation of polyunsaturated fatty acids and sterols in solution and in liposomes J. Am. Chem. Soc. 131 2009 13037 13044
15. L. Xu, Z. Korade, and N.A. Porter Oxysterols from free radical chain oxidation of 7-dehydrocholesterol: product and mechanistic studies J. Am. Chem. Soc. 132 2010 2222 2232
16. Z. Korade, L. Xu, R. Shelton, and N.A. Porter Biological activities of 7-dehydrocholesterol-derived oxysterols: implications for Smith-Lemli-Opitz syndrome J. Lipid Res. 51 2010 3259 3269
17. L. Xu, Z. Korade, D.A. Rosado, W. Liu, C.R. Lamberson, and N.A. Porter An oxysterol biomarker for 7-dehydrocholesterol oxidation in cell/mouse models for Smith-Lemli-Opitz syndrome J. Lipid Res. 52 2011 1222 1233
18. G.J. Schroepfer Jr. Oxysterols: modulators of cholesterol metabolism and other processes Physiol. Rev. 80 2000 361 554 (Pubitemid 30060568)
19. A. Vejux, and G. Lizard Cytotoxic effects of oxysterols associated with human diseases: induction of cell death (apoptosis and/or oncosis), oxidative and inflammatory activities, and phospholipidosis Mol. Aspects Med. 30 2009 153 170
20. A.J. Brown, and W. Jessup Oxysterols: sources, cellular storage and metabolism, and new insights into their roles in cholesterol homeostasis Mol. Aspects Med. 30 2009 111 122
21. B.U. Fitzky, F.F. Moebius, H. Asaoka, H. Waage-Baudet, L. Xu, G. Xu, N. Maeda, K. Kluckman, S. Hiller, H. Yu, A.K. Batta, S. Shefer, T. Chen, G. Salen, K. Sulik, R.D. Simoni, G.C. Ness, H. Glossmann, S.B. Patel, and G.S. Tint 7-Dehydrocholesterol-dependent proteolysis of HMG-CoA reductase suppresses sterol biosynthesis in a mouse model of Smith-Lemli-Opitz/RSH syndrome J. Clin. Invest. 108 2001 905 915 (Pubitemid 32880299)
22. C.A. Wassif, P. Zhu, L. Kratz, P.A. Krakowiak, K.P. Battaile, F.F. Weight, A. Grinberg, R.D. Steiner, N.A. Nwokoro, R.I. Kelley, R.R. Stewart, and F.D. Porter Biochemical, phenotypic and neurophysiological characterization of a genetic mouse model of RSH/Smith-Lemli-Opitz syndrome Hum. Mol. Genet. 10 2001 555 564 (Pubitemid 32229359)
23. M. Kolf-Clauw, F. Chevy, C. Wolf, B. Siliart, D. Citadelle, and C. Roux Inhibition of 7-dehydrocholesterol reductase by the teratogen AY9944: a rat model for Smith-Lemli-Opitz syndrome Teratology 54 1996 115 125 (Pubitemid 27042473)
24. G. Xu, G. Salen, S. Shefer, G.C. Ness, T.S. Chen, Z. Zhao, and G.S. Tint Reproducing abnormal cholesterol biosynthesis as seen in the Smith-Lemli-Opitz syndrome by inhibiting the conversion of 7-dehydrocholesterol to cholesterol in rats J. Clin. Invest. 95 1995 76 81
25. S.J. Fliesler, M.J. Richards, C. Miller, and N.S. Peachey Marked alteration of sterol metabolism and composition without compromising retinal development or function Invest. Ophthalmol. Vis. Sci. 40 1999 1792 1801 (Pubitemid 29297156)
26. S.J. Fliesler, N.S. Peachey, M.J. Richards, B.A. Nagel, and D.K. Vaughan Retinal degeneration in a rodent model of Smith-Lemli-Opitz syndrome: electrophysiologic, biochemical, and morphologic features Arch. Ophthalmol. 122 2004 1190 1200 (Pubitemid 39031136)
27. S.J. Fliesler, D.K. Vaughan, E.C. Jenewein, M.J. Richards, B.A. Nagel, and N.S. Peachey Partial rescue of retinal function and sterol steady-state in a rat model of Smith-Lemli-Opitz syndrome Pediatr. Res. 61 2007 273 278
28. M.J. Richards, B.A. Nagel, and S.J. Fliesler Lipid hydroperoxide formation in the retina: correlation with retinal degeneration and light damage in a rat model of Smith-Lemli-Opitz syndrome Exp. Eye Res. 82 2006 538 541 (Pubitemid 43138968)
29. D.K. Vaughan, N.S. Peachey, M.J. Richards, B. Buchan, and S.J. Fliesler Light-induced exacerbation of retinal degeneration in a rat model of Smith-Lemli-Opitz syndrome Exp. Eye Res. 82 2006 496 504 (Pubitemid 43138964)
30. L. Xu, W. Liu, L.G. Sheflin, S.J. Fliesler, and N.A. Porter Novel oxysterols observed in tissues and fluids of AY9944-treated rats - a model for Smith-Lemli-Opitz syndrome J. Lipid Res. 52 2011 1810 1820
31. R. Shinkyo, L. Xu, K.A. Tallman, Q. Cheng, N.A. Porter, and F.P. Guengerich Conversion of 7-dehydrocholesterol to 7-ketocholesterol is catalyzed by human cytochrome P450 7A1 and occurs by direct oxidation without an epoxide intermediate J. Biol. Chem. 286 2011 33021 33028
32. S.J. Fliesler Retinal degeneration in a rat model of Smith-Lemli-Opitz syndrome: thinking beyond cholesterol deficiency Adv. Exp. Med. Biol. 664 2010 481 489
33. S.J. Fliesler, and L. Bretillon The ins and outs of cholesterol in the vertebrate retina J. Lipid Res. 51 2010 3399 3413
34. S.J. Fliesler, and R.E. Anderson Chemistry and metabolism of lipids in the vertebrate retina Prog. Lipid Res. 22 1983 79 131
35. P. Palozza, S. Serini, S. Verdecchia, M. Ameruso, S. Trombino, N. Picci, G. Monego, and F.O. Ranelletti Redox regulation of 7-ketocholesterol-induced apoptosis by beta-carotene in human macrophages Free Radical Biol. Med. 42 2007 1579 1590 (Pubitemid 46590620)
36. W. Baehr, and J.M. Frederick Naturally occurring animal models with outer retina phenotypes Vision Res. 49 2009 2636 2652
37. E.L. Fletcher, A.I. Jobling, K.A. Vessey, C. Luu, R.H. Guymer, and P.N. Baird Animal models of retinal disease Prog. Mol. Biol. Transl. Sci. 100 2011 211 286
38. K. Bodin, L. Bretillon, Y. Aden, L. Bertilsson, U. Broome, C. Einarsson, and U. Diczfalusy Antiepileptic drugs increase plasma levels of 4beta-hydroxycholesterol in humans: evidence for involvement of cytochrome p450 3A4 J. Biol. Chem. 276 2001 38685 38689
39. E.G. Lund, J.M. Guileyardo, and D.W. Russell cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain Proc. Natl. Acad. Sci. U. S. A. 96 1999 7238 7243 (Pubitemid 29299645)
40. I.A. Pikuleva Cytochrome P450s and cholesterol homeostasis Pharmacol. Ther. 112 2006 761 773 (Pubitemid 44573496)
41. G. Stapleton, M. Steel, M. Richardson, J.O. Mason, K.A. Rose, R.G. Morris, and R. Lathe A novel cytochrome P450 expressed primarily in brain J. Biol. Chem. 270 1995 29739 29745 (Pubitemid 26001640)
42. K.A. Rose, G. Stapleton, K. Dott, M.P. Kieny, R. Best, M. Schwarz, D.W. Russell, I. Bjorkhem, J. Seckl, and R. Lathe Cyp7b, a novel brain cytochrome P450, catalyzes the synthesis of neurosteroids 7alpha-hydroxy dehydroepiandrosterone and 7alpha-hydroxy pregnenolone Proc. Natl. Acad. Sci. U. S. A. 94 1997 4925 4930 (Pubitemid 27214712)
43. S.J. Fliesler, R. Florman, L.M. Rapp, S.J. Pittler, and R.K. Keller In vivo biosynthesis of cholesterol in the rat retina FEBS Lett. 335 1993 234 238 (Pubitemid 23350413)
44. S.J. Fliesler, and R.K. Keller Metabolism of [3H]farnesol to cholesterol and cholesterogenic intermediates in the living rat eye Biochem. Biophys. Res. Commun. 210 1995 695 702
45. S.J. Fliesler, M.J. Richards, C. Miller, N.S. Peachey, and R.J. Cenedella Retinal structure and function in an animal model that replicates the biochemical hallmarks of desmosterolosis Neurochem. Res. 25 2000 685 694 (Pubitemid 30422003)
46. S.J. Fliesler, M.J. Richards, C.Y. Miller, and R.J. Cenedella Cholesterol synthesis in the vertebrate retina: effects of U18666A on rat retinal structure, photoreceptor membrane assembly, and sterol metabolism and composition Lipids 35 2000 289 296 (Pubitemid 30198774)
47. N. Tserentsoodol, N.V. Gordiyenko, I. Pascual, J.W. Lee, S.J. Fliesler, and I.R. Rodriguez Intraretinal lipid transport is dependent on high density lipoprotein-like particles and class B scavenger receptors Mol. Vis. 12 2006 1319 1333 (Pubitemid 44688463)
48. I.R. Rodriguez, and S.J. Fliesler Photodamage generates 7-keto- and 7-hydroxycholesterol in the rat retina via a free radical-mediated mechanism Photochem. Photobiol. 85 2009 1116 1125
49. L. Xu, K. Mirnics, A.B. Bowman, W. Liu, J. Da, N.A. Porter, and Z. Korade DHCEO accumulation is a critical mediator of pathophysiology in a Smith-Lemli-Opitz syndrome model Neurobiol. Dis. 2011 Epub ahead of print; December 11, 2011; DOI: 2010.1016/j.nbd.2011.2012.2011
50. A.J. Brown, S.L. Leong, R.T. Dean, and W. Jessup 7-Hydroperoxycholesterol and its products in oxidized low density lipoprotein and human atherosclerotic plaque J. Lipid Res. 38 1997 1730 1745 (Pubitemid 27411265)
51. I.R. Rodriguez, and I.M. Larrayoz Cholesterol oxidation in the retina: implications of 7KCh formation in chronic inflammation and age-related macular degeneration J. Lipid Res. 51 2010 2847 2862
52. P. Singh, Y.D. Paila, and A. Chattopadhyay Differential effects of cholesterol and 7-dehydrocholesterol on the ligand binding activity of the hippocampal serotonin(1A) receptor: implications in SLOS Biochem. Biophys. Res. Commun. 358 2007 495 499 (Pubitemid 46755732)
53. A. Chattopadhyay, Y.D. Paila, M. Jafurulla, A. Chaudhuri, P. Singh, M.R. Murty, and M. Vairamani Differential effects of cholesterol and 7-dehydrocholesterol on ligand binding of solubilized hippocampal serotonin1A receptors: implications in SLOS Biochem. Biophys. Res. Commun. 363 2007 800 805 (Pubitemid 47513700)
54. Y.D. Paila, M.R. Murty, M. Vairamani, and A. Chattopadhyay Signaling by the human serotonin(1A) receptor is impaired in cellular model of Smith-Lemli-Opitz syndrome Biochim. Biophys. Acta 1778 2008 1508 1516
55. J.B. Massey Membrane and protein interactions of oxysterols Curr. Opin. Lipidol. 17 2006 296 301 (Pubitemid 43786065)
56. V.M. Olkkonen, and R. Hynynen Interactions of oxysterols with membranes and proteins Mol. Aspects Med. 30 2009 123 133
57. H. Girao, M.C. Mota, J. Ramalho, and P. Pereira Cholesterol oxides accumulate in human cataracts Exp. Eye Res. 66 1998 645 652 (Pubitemid 28267134)
58. A.L. Gramajo, L.C. Zacharias, A. Neekhra, S. Luthra, S.R. Atilano, M. Chwa, D.J. Brown, B.D. Kuppermann, and M.C. Kenney Mitochondrial DNA damage induced by 7-ketocholesterol in human retinal pigment epithelial cells in vitro Invest. Ophthalmol. Vis. Sci. 51 2010 1164 1170