Probing lipid-protein adduction with alkynyl surrogates: Application to Smith-Lemli-Opitz syndrome

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2842-2850

  Windsor, Katherine ^a   Genaro Mattos, Thiago C ^a,b   Kim, Hye Young H ^a,c   Liu, Wei ^a   Tallman, Keri A ^a   Miyamoto, Sayuri ^b   Korade, Zeljka ^a,d   Porter, Ned A ^a,c,d  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

7 dehydrocholesterol; Cholesterol; Lipid electrophiles; Lipid peroxidation; Oxysterol

Indexed keywords

7 DEHYDROCHOLESTEROL; ALKYNYL GROUP; CHOLESTEROL; OXYSTEROL; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; PROTEOME;

ARTICLE; BIOTINYLATION; CELL METABOLISM; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE MARKER; LIPID ANALYSIS; LIPID PEROXIDATION; LIPOGENESIS; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PHYSICAL PHENOMENA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LIPID ADDUCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; SMITH LEMLI OPITZ SYNDROME; TREND STUDY; WESTERN BLOTTING;

7-DEHYDROCHOLESTEROL; CHOLESTEROL; LIPID ELECTROPHILES; LIPID PEROXIDATION; OXYSTEROL;

CELL LINE, TUMOR; CYTOCHROMES C; DEHYDROCHOLESTEROLS; FATTY ACIDS, UNSATURATED; HUMANS; LIPOYLATION; OXIDATION-REDUCTION; PHOSPHOLIPIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SMITH-LEMLI-OPITZ SYNDROME;

EID: 84884168586     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M041061     Document Type: Article

References (47)

1. Nadolski, M. J., and M. E. Linder. 2007. Protein lipidation. FEBS J. 274: 5202-5210.
2. Hang, H. C., and M. E. Linder. 2011. Exploring protein lipidation with chemical biology. Chem. Rev. 111: 6341-6358.
3. Resh, M. D. 2012. Targeting protein lipidation in disease. Trends Mol. Med. 18: 206-214.
4. Triola, G., H. Waldmann, and C. Hedberg. 2012. chemical biology of lipidated proteins. ACS Chem. Biol. 7: 87-99.
5. Nes, W. D. 2011. Biosynthesis of cholesterol and other sterols. Chem. Rev. 111: 6423-6451.
6. Xu, L., T. A. Davis, and N. A. Porter. 2009. Rate constants for peroxidation of polyunsaturated fatty acids and sterols in solution and in liposomes. J. Am. Chem. Soc. 131: 13037-13044.
7. Tint, G. S., M. Seller, R. Hughes-Benzie, A. K. Batta, S. Shefer, D. Genest, M. Irons, E. Elias, and G. Salen. 1995. Markedly increased tissue concentrations of 7-dehydrocholesterol combined with low levels of cholesterol are characteristic of the Smith-Lemli-Opitz syndrome. J. Lipid Res. 36: 89-95.
8. Porter, F. D., and G. E. Herman. 2011. Malformation syndromes caused by disorders of cholesterol synthesis. J. Lipid Res. 52: 6-34.
9. Kelley, R. I., and R. C. M. Hennekam. 2000. The Smith-Lemli-Opitz syndrome. J. Med. Genet. 37: 321-335.
10. Lee, R. W. Y., and E. Tierney. 2011. Hypothesis: the role of sterols in autism spectrum disorder. Autism Res. Treat. 2011: 653570.
11. Sikora, D. M., K. Pettit-Kekel, J. Penfield, L. S. Merkens, and R. D. Steiner. 2006. The near universal presence of autism spectrum disorders in children with Smith-Lemli-Opitz syndrome. Am. J. Med. Genet. A. 140: 1511-1518.
12. Gaoua, W., F. Chevy, C. Roux, and C. Wolf. 1999. Oxidized derivatives of 7-dehydrocholesterol induce growth retardation in cultured rat embryos: a model for antenatal growth retardation in the Smith- Lemli-Opitz syndrome. J. Lipid Res. 40: 456-463.
13. Richards, M. J., B. A. Nagel, and S. J. Fliesler. 2006. 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: 538-541.
14. Valencia, A., A. Rajadurai, A. B. Carle, and I. E. Kochevar. 2006. 7-Dehydrocholesterol enhances ultraviolet A-induced oxidative stress in keratinocytes: roles of NADPH oxidase, mitochondria, and lipid rafts. Free Radic. Biol. Med. 41: 1704-1718.
15. Xu, L., Z. Korade, and N. A. Porter. 2010. Oxysterols from free radical chain oxidation of 7-dehydrocholesterol: product and mechanistic studies. J. Am. Chem. Soc. 132: 2222-2232.
16. Xu, L., Z. Korade, D. A. Rosado, W. Liu, C. R. Lamberson, and N. A. Porter. 2011. An oxysterol biomarker for 7-dehydrocholesterol oxidation in cell/mouse models for Smith-Lemli-Opitz syndrome. J. Lipid Res. 52: 1222-1233.
17. Xu, L., W. Liu, L. G. Sheflin, S. J. Fliesler, and N. A. Porter. 2011. Novel oxysterols observed in tissues and fluids of AY9944-treated rats: a model for Smith-Lemli-Opitz syndrome. J. Lipid Res. 52: 1810-1820.
18. Xu, L., Z. Korade, D. A. Rosado, K. Mirnics, and N. A. Porter. 2013. Metabolism of oxysterols derived from nonenzymatic oxidation of 7-dehydrocholesterol in cells. J. Lipid Res. 54: 1135-1143.
19. Schneider, C., N. A. Porter, and A. R. Brash. 2008. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J. Biol. Chem. 283: 15539-15543.
20. Sayre, L. M., D. Lin, Q. Yuan, X. Zhu, and X. Tang. 2006. Protein adducts generated from products of lipid oxidation: focus on HNE and ONE. Drug Metab. Rev. 38: 651-675.
21. Vila, A., K. A. Tallman, A. T. Jacobs, D. C. Liebler, N. A. Porter, and L. J. Marnett. 2008. Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives. Chem. Res. Toxicol. 21: 432-444.
22. Codreanu, S. G., B. Zhang, S. M. Sobecki, D. D. Billheimer, and D. C. Liebler. 2009. Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal. Mol. Cell. Proteomics. 8: 670-680.
23. Perluigi, M., R. Coccia, and D. A. Butterfield. 2012. 4-Hydroxy-2- nonenal, a reactive product of lipid peroxidation, and neurodegenerative diseases: a toxic combination illuminated by redox proteomics studies. Antioxid. Redox Signal. 17: 1590-1609.
24. Zarkovic, K. 2003. 4-Hydroxynonenal and neurodegenerative diseases. Mol. Aspects Med. 24: 293-303.
25. Leonarduzzi, G., E. Chiarpotto, F. Biasi, and G. Poli. 2005. 4-Hydroxynonenal and cholesterol oxidation products in atherosclerosis. Mol. Nutr. Food Res. 49: 1044-1049.
26. Jacobs, A. T., and L. J. Marnett. 2010. Systems analysis of protein modification and cellular responses induced by electrophile stress. Acc. Chem. Res. 43: 673-683.
27. Kim, H-Y. H., K. A. Tallman, D. C. Liebler, and N. A. Porter. 2009. An azido-biotin reagent for use in the isolation of protein adducts of lipid-derived electrophiles by streptavidin catch and photorelease. Mol. Cell. Proteomics. 8: 2080-2089.
28. Milne, S. B., K. A. Tallman, R. Serwa, C. A. Rouzer, M. D. Armstrong, L. J. Marnett, C. M. Lukehart, N. A. Porter, and H. A. Brown. 2010. Capture and release of alkyne-derivatized glycerophospholipids using cobalt chemistry. Nat. Chem. Biol. 6: 205-207.
29. Tallman, K. A., M. D. Armstrong, S. B. Milne, L. J. Marnett, H. A. Brown, and N. A. Porter. 2013. Cobalt carbonyl complexes as probes for alkyne-tagged lipids. J. Lipid Res. 54: 859-868.
30. Rostovtsev, V. V., L. G. Green, V. V. Fokin, and K. B. Sharpless. 2002. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41: 2596-2599.
31. Thirumurugan, P., D. Matosiuk, and K. Jozwiak. 2013. Click chemistry for drug development and diverse chemical-biology applications. Chem. Rev. 113: 4905-4979.
32. Liu, W., L. Xu, C. R. Lamberson, L. S. Merkens, R. D. Steiner, E. R. Elias, D. Haas, and N. A. Porter. 2013. Assays of plasma dehydrocholesteryl esters and oxysterols from Smith-Lemli-Opitz syndrome patients. J. Lipid Res. 54: 244-253.
33. Hong, V., S. I. Presolski, C. Ma, and M. G. Finn. 2009. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. Engl. 48: 9879-9883.
34. McComsey, D. F., A. B. Reitz, C. A. Maryanoff, and B. E. Maryanoff. 1986. Deoxygenation of acetylenic carbinols. reduction of cobalt carbonyl adducts with borane-methyl sulfide and trifluoroacetic acid. Synth. Commun. 16: 1535-1549.
35. Aluise, C. D., K. Rose, M. Boiani, M. L. Reyzer, J. D. Manna, K. Tallman, N. A. Porter, and L. J. Marnett. 2013. Peptidyl-prolyl cis/trans-isomerase A1 (Pin1) Is a target for modification by lipid electrophiles. Chem. Res. Toxicol. 26: 270-279.
36. Witsch-Baumgartner, M., J. Löffler, and G. Utermann. 2001. Mutations in the human DHCR7 gene. Hum. Mutat. 17: 172-182.
37. Korade, Z., A. K. Kenworthy, and K. Mirnics. 2009. Molecular consequences of altered neuronal cholesterol biosynthesis. J. Neurosci. Res. 87: 866-875.
38. Liang, X., A. Nazarian, H. Erdjument-Bromage, W. Bornmann, P. Tempst, and M. D. Resh. 2001. Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J. Biol. Chem. 276: 30987-30994.
39. Ekkebus, R., S. I. van Kasteren, Y. Kulathu, A. Scholten, I. Berlin, P. P. Geurink, A. de Jong, S. Goerdayal, J. Neefjes, A. J. R. Heck, et al. 2013. On terminal alkynes that can react with active-site cysteine nucleophiles in proteases. J. Am. Chem. Soc. 135: 2867-2870.
40. Cygan, N. K., J. C. Scheinost, T. D. Butters, and P. Wentworth. 2011. Adduction of cholesterol 5,6-secosterol aldehyde to membranebound myelin basic protein exposes an immunodominant epitope. Biochemistry. 50: 2092-2100.
41. Nieva, J., A. Shafton, L. J. Altobell, S. Tripuraneni, J. K. Rogel, A. D. Wentworth, R. A. Lerner, and P. Wentworth. 2008. Lipid-derived aldehydes accelerate light chain amyloid and amorphous aggregation. Biochemistry. 47: 7695-7705.
42. Zhang, Q., E. T. Powers, J. Nieva, M. E. Huff, M. A. Dendle, J. Bieschke, C. G. Glabe, A. Eschenmoser, P. Wentworth, R. A. Lerner, et al. 2004. Metabolite-initiated protein misfolding may trigger Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 101: 4752-4757.
43. Bosco, D. A., D. M. Fowler, Q. Zhang, J. Nieva, E. T. Powers, P. Wentworth, Jr ., R. A. Lerner, and J. W. Kelly. 2006. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat. Chem. Biol. 2: 249-253.
44. Korade, Z., L. Xu, R. Shelton, and N. A. Porter. 2010. Biological activities of 7-dehydrocholesterol-derived oxysterols: implications for Smith-Lemli-Opitz syndrome. J. Lipid Res. 51: 3259-3269.
45. Xu, L., K. Mirnics, A. B. Bowman, W. Liu, J. Da, N. A. Porter, and Z. Korade. 2012. DHCEO accumulation is a critical mediator of pathophysiology in a Smith-Lemli-Opitz syndrome model. Neurobiol. Dis. 45: 923-929.
46. Payré, B., P. de Medina, N. Boubekeur, L. Mhamdi, J. Bertrand- Michel, F. Tercé, I. Fourquaux, D. Goudounèche, M. Record, M. Poirot, et al. 2008. Microsomal antiestrogen-binding site ligands induce growth control and differentiation of human breast cancer cells through the modulation of cholesterol metabolism. Mol. Cancer Ther. 7: 3707-3718.
47. de Sain-van der Velden, M. G. M., A. Verrips, B. H. C. M. T. Prinsen, M. de Barse, R. Berger, and G. Visser. 2008. Elevated cholesterol precursors other than cholestanol can also be a hallmark for CTX. J. Inherit. Metab. Dis. 31(Suppl. 2): S 387 -S 393.