Cytochrome P450 2C epoxygenases mediate photochemical stress-induced death of photoreceptors

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8337-8352

  Chang, Qing ^a   Berdyshev, Evgeny ^a   Cao, Dingcai ^a   Bogaard, Joseph D ^a   White, Jerry J ^a   Chen, Siquan ^b   Shah, Ravi ^a   Mu, Wenbo ^a   Grantner, Rita ^b   Bettis, Sam ^b   Grassi, Michael A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CHEMICAL COMPOUNDS; CHROMOPHORES; GENES; METABOLITES; OPHTHALMOLOGY; PHOSPHOLIPIDS; PROTEINS; TUNGSTEN COMPOUNDS; UNSATURATED FATTY ACIDS;

AGE-RELATED MACULAR DEGENERATION; CONDENSATION PRODUCT; HIGH-THROUGHPUT SCREENS; MEMBRANE PHOSPHOLIPIDS; RETINAL DEGENERATIVE DISEASE; RETINITIS PIGMENTOSA; SELECTIVE INHIBITORS; STABLE EXPRESSION;

VISION;

ARACHIDONIC ACID; CYTOCHROME P450 2C; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; SULFAPHENAZOLE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CHROMATOPHORE; CONTROLLED STUDY; CYP2C GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HIGH THROUGHPUT SCREENING; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHOTOCHEMISTRY; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINITIS PIGMENTOSA; SENSITIVITY ANALYSIS;

APOPTOSIS; CALCIUM; CYTOCHROME P450; DRUG SCREENING; EICOSANOID; FATTY ACID; NECROSIS (NECROTIC DEATH);

AMINO ACID SEQUENCE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CELL DEATH; CELL LINE; CYTOCHROME P-450 ENZYME SYSTEM; CYTOPROTECTION; DRUG EVALUATION, PRECLINICAL; GENE EXPRESSION; GENE SILENCING; HUMANS; LIGHT; MICE; MOLECULAR SEQUENCE DATA; PHOTORECEPTOR CELLS, VERTEBRATE; SEQUENCE ALIGNMENT; SULFAPHENAZOLE;

EID: 84896933315     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507152     Document Type: Article

References (90)

1. Buch, H., Vinding, T., La Cour, M., Appleyard, M., Jensen, G. B., and Nielsen, N. V. (2004) Prevalence and causes of visual impairment and blindness among 9980 Scandinavian adults: the Copenhagen City Eye Study. Ophthalmology 111, 53-61 (Pubitemid 38032210)
2. Al-Merjan, J. I., Pandova, M. G., Al-Ghanim M, Al-Wayel, A., and Al-Mutairi S (2005) Registered blindness and low vision in Kuwait. Ophthalmic Epidemiol. 12, 251-257 (Pubitemid 41702807)
3. Hata, H., Yonezawa, M., Nakanishi, T., Ri, T., and Yanashima, K. (2003) Causes of entering institutions for visually handicapped persons during the past fifteen years. Jpn. J. Ophthalmol. 57, 259-262 (Pubitemid 36422882)
4. Frick, K. D., Roebuck, M. C., Feldstein, J. I., McCarty, C. A., and Grover, L. L. (2012) Health services utilization and cost of retinitis pigmentosa. Arch. Ophthalmol. 130, 629-634
5. Friedman, D. S., O'Colmain, B. J., Muñoz, B., Tomany, S. C., McCarty, C., de Jong, P. T., Nemesure, B., Mitchell, P., Kempen, J., and Eye Diseases Prevalence Research Group (2004) Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 122, 564-572 (Pubitemid 38456293)
6. Congdon, N., O'Colmain, B., Klaver, C. C., Klein, R., Muñoz, B., Friedman, D. S., Kempen, J., Taylor, H. R., Mitchell, P., and Eye Diseases Prevalence Research Group (2004) Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 122, 477-485 (Pubitemid 38456282)
7. Bressler, S. B., Muñoz, B., Solomon, S. D., West, S. K., and Salisbury Eye Evaluation (SEE) Study Team (2008) Racial differences in the prevalence of age-related macular degeneration: the Salisbury Eye Evaluation (SEE) Project. Arch. Ophthalmol. 126, 241-245 (Pubitemid 351240854)
8. Faktorovich, E. G., Steinberg, R. H., Yasumura, D., Matthes, M. T., and LaVail, M. M. (1990) Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature 347, 83-86
9. Frasson, M., Picaud, S., Léveillard, T., Simonutti, M., Mohand-Said, S., Dreyfus, H., Hicks, D., and Sabel, J. (1999) Glial cell line-derived neurotrophic factor induces histologic and functional protection of rod photoreceptors in the rd/rd mouse. Invest. Ophthalmol. Vis. Sci. 40, 2724-2734 (Pubitemid 29455505)
10. Cayouette, M., Behn, D., Sendtner, M., Lachapelle, P., and Gravel, C. (1998) Intraocular gene transfer of ciliary neurotrophic factor prevents death and increases responsiveness of rod photoreceptors in the retinal degeneration slow mouse. J. Neurosci. 18, 9282-9293 (Pubitemid 28512459)
11. Koch, S., Sothilingam, V., Garcia Garrido, M., Tanimoto, N., Becirovic, E., Koch, F., Seide, C., Beck, S. C., Seeliger, M. W., Biel, M., Mühlfriedel, R., and Michalakis, S. (2012) Gene therapy restores vision and delays degeneration in the CNGB1-/- mouse model of retinitis pigmentosa. Hum. Mol. Genet. 21, 4486-4496
12. Pang, J. J., Boye, S. L., Kumar, A., Dinculescu, A., Deng, W., Li, J., Li, Q., Rani, A., Foster, T. C., Chang, B., Hawes, N. L., Boatright, J. H., and Hauswirth, W. W. (2008) AAV-mediated gene therapy for retinal degeneration in the rd10 mouse containing a recessive PDEβ mutation. Invest. Ophthalmol. Vis. Sci. 49, 4278-4283
13. Komeima, K., Rogers, B. S., Lu, L., and Campochiaro, P. A. (2006) Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 103, 11300-11305 (Pubitemid 44159928)
14. Otani, A., Dorrell, M. I., Kinder, K., Moreno, S. K., Nusinowitz, S., Banin, E., Heckenlively, J., and Friedlander, M. (2004) Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J. Clin. Investig. 114, 765-774 (Pubitemid 39578735)
15. Berson, E. L., Rosner, B., Sandberg, M. A., Hayes, K. C., Nicholson, B. W., Weigel-DiFranco, C., and Willett, W. (1993) A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch. Ophthalmol. 111, 761-772 (Pubitemid 23170587)
16. Radu, R. A., Yuan, Q., Hu, J., Peng, J. H., Lloyd M, Nusinowitz, S., Bok, D., and Travis, G. H. (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, 3821-3829
17. Rosenfeld, P. J., Brown, D. M., Heier, J. S., Boyer, D. S., Kaiser, P. K., Chung, C. Y., Kim, R. Y., and MARINA Study Group. (2006) Ranibizumab for neovascular age-related macular degeneration. N. Engl. J. Med. 355, 1419-1431 (Pubitemid 44511557)
18. Hollyfield, J. G., Bonilha, V. L., Rayborn, M. E., Yang, X., Shadrach, K. G., Lu, L., Ufret, R. L., Salomon, R. G., and Perez, V. L. (2008) Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat. Med. 14, 194-198 (Pubitemid 351214555)
19. Ding, X., Patel, M., and Chan, C. C. (2009) Molecular pathology of age-related macular degeneration. Prog. Retin. Eye Res. 28, 1-18
20. Chew, E. Y., Clemons, T. E., Agrón, E., Sperduto, R. D., Sangiovanni, J. P., Kurinij, N., Davis, M. D., and Age-Related Eye Disease Study Research Group. (2013) Long-term effects of vitamins C and E, β-carotene, and zinc on age-related macular degeneration: AREDS Report No. 35. Ophthalmology 120, 1604-11.e4
21. Pollitt, S. K., Pallos, J., Shao, J., Desai, U. A., Ma, A. A., Thompson, L. M., Marsh, J. L., and Diamond, M. I. (2003) A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor. Neuron 40, 685-694 (Pubitemid 37431030)
22. Bush, E., Fielitz, J., Melvin, L., Martinez-Arnold, M., McKinsey, T. A., Plichta, R., and Olson, E. N. (2004) A small molecular activator of cardiac hypertrophy uncovered in a chemical screen for modifiers of the calcineurin signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 2870-2875 (Pubitemid 38327703)
23. Gupta, P. B., Onder, T. T., Jiang, G., Tao, K., Kuperwasser, C., Weinberg, R. A., and Lander, E. S. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645-659
24. Somwar, R., Shum, D., Djaballah, H., and Varmus, H. (2009) Identification and preliminary characterization of novel small molecules that inhibit growth of human lung adenocarcinoma cells. J. Biomol. Screen 14, 1176-1184
25. Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G. D., Mitchison, T. J., Moskowitz, M. A., and Yuan, J. (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112-119
26. Kepp, O., Galluzzi, L., Lipinski, M., Yuan, J., and Kroemer, G. (2011) Cell death assays for drug discovery. Nat. Rev. Drug Discov. 10, 221-237
27. Paskowitz, D. M., LaVail, M. M., and Duncan, J. L. (2006) Light and inherited retinal degeneration. Br. J. Ophthalmol. 90, 1060-1066 (Pubitemid 44140192)
28. Kijas, J. W., Cideciyan, A. V., Aleman, T. S., Pianta M. J., Pearce-Kelling, S. E., Miller, B. J., Jacobson, S. G., Aguirre, G. D., and Acland, G. M. (2002) Naturally occurring rhodopsin mutation in the dog causes retinal dysfunction and degeneration mimicking human dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 99, 6328-6333 (Pubitemid 34493311)
29. Naash, M. L., Peachey, N. S., Li, Z. Y., Gryczan, C. C., Goto, Y., Blanks, J., Milam, A. H., and Ripps, H. (1996) Light induced acceleration of photoreceptor degeneration in transgenic mice expressing mutant rhodopsin. Invest. Ophthalmol. Vis. Sci. 37, 775-782 (Pubitemid 26110430)
30. Wenzel, A., Grimm, C., Samardzija, M., and Remé, C. E. (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog. Retin. Eye Res. 24, 275-306 (Pubitemid 40021788)
31. Marc, R. E., Jones, B. W., Watt, C. B., Vazquez-Chona, F., Vaughan, D. K., and Organisciak, D. T. (2008) Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol. Vis. 14, 782-806 (Pubitemid 351780862)
32. Rutar, M., Provis, J. M., and Valter, K. (2010) Brief exposure to damaging light causes focal recruitment of macrophages, and long-term destabilization of photoreceptors in the albino rat retina. Curr. Eye Res. 35, 631-643
33. Rutar, M., Natoli, R., Kozulin, P., Valter, K., Gatenby, P., and Provis, J. M. (2011) Analysis of complement expression in light-induced retinal degeneration: synthesis and deposition of C3 by microglia/macrophages is associated with focal photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci. 52, 5347-5358
34. Chang, Q., Peter, M. E., and Grassi, M. A. (2012) Fas ligand-Fas signaling participates in light-induced apoptotic death in photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 53, 3703-3716
35. Zhang, J. H., Chung, T. D., and Oldenburg, K. R. (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4, 67-73 (Pubitemid 29278954)
36. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
37. Farber, D. B. (1995) From mice to men: the cyclic GMP phosphodiesterase gene in vision and disease. Invest. Ophthalmol. Vis. Sci. 36, 263-275
38. Barabas, P., Cutler Peck, C., and Krizaj, D. (2010) Do calcium channel blockers rescue dying photoreceptors in the Pde6b (rd1) mouse? Adv. Exp. Med. Biol. 664, 491-499
39. Wu, H., Cowing, J. A., Michaelides, M., Wilkie, S. E., Jeffery, G., Jenkins, S. A., Mester, V., Bird, A. C., Robson, A. G., Holder, G. E., Moore, A. T., Hunt, D. M., and Webster, A. R. (2006) Mutations in the gene KCNV2 encoding a voltage-gated potassium channel subunit cause "cone dystrophy with supernormal rod electroretinogram" in humans. Am. J. Hum. Genet. 79, 574-579 (Pubitemid 44384268)
40. Babai, N., and Thoreson, W. B. (2009) Horizontal cell feedback regulates calcium currents and intracellular calcium levels in rod photoreceptors of salamander and mouse retina. J. Physiol. 587, 2353-2364
41. Ogilvie, J. M., and Speck, J. D. (2002) Dopamine has a critical role in photoreceptor degeneration in the rd mouse. Neurobiol. Dis. 10, 33-40 (Pubitemid 34757080)
42. Bubenik, G. A., and Purtill, R. A. (1980) The role of melatonin and dopamine in retinal physiology. Can. J. Physiol. Pharmacol. 58, 1457-1462 (Pubitemid 11146505)
43. Wiechmann, A. F., and O'Steen, W. K. (1992) Melatonin increases photo-receptor susceptibility to light-induced damage. Invest. Ophthalmol. Vis. Sci. 33, 1894-1902
44. Sugawara, T., Sieving, P. A., Iuvone, P. M., and Bush, R. A. (1998) The melatonin antagonist luzindole protects retinal photoreceptors from light damage in the rat. Invest. Ophthalmol. Vis. Sci. 39, 2458-2465 (Pubitemid 28485657)
45. Nguyen-Legros, J., Chanut, E., Versaux-Botteri, C., Simon, A., and Trouvin, J. H. (1996) Dopamine inhibits melatonin synthesis in photoreceptor cells through a D2-like receptor subtype in the rat retina: biochemical and histochemical evidence. J. Neurochem. 67, 2514-2520 (Pubitemid 26392523)
46. Cohen, A. I., Todd, R. D., Harmon, S., and O'Malley, K. L. (1992) Photo-receptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 89, 12093-12097 (Pubitemid 23004791)
47. Wenzel, A., Grimm, C., Seeliger, M. W., Jaissle, G., Hafezi, F., Kretschmer, R., Zrenner, E., and Remé, C. E. (2001) Prevention of photoreceptor apoptosis by activation of the glucocorticoid receptor. Invest. Ophthalmol. Vis. Sci. 42, 1653-1659 (Pubitemid 32520761)
48. Zhang, C., Lei, B., Lam, T. T., Yang, F., Sinha, D., and Tso, M. O. (2004) Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest. Ophthalmol. Vis. Sci. 45, 2753-2759 (Pubitemid 38998874)
49. Yang, L. P., Zhu, X. A., and Tso, M. O. (2007) A possible mechanism of microglia-photoreceptor crosstalk. Mol. Vis. 13, 2048-2057
50. Biber, K., Neumann, H., Inoue, K., and Boddeke, H. W. (2007) Neuronal 'on' and 'off' signals control microglia. Trends Neurosci. 30, 596-602 (Pubitemid 350051426)
51. Chen, Y., Okano, K., Maeda, T., Chauhan, V., Golczak, M., Maeda, A., and Palczewski, K. (2012) Mechanism of all-trans-retinal toxicity with implications for Stargardt disease and age-related macular degeneration. J. Biol. Chem. 287, 5059-5069
52. Bursch, W., Hochegger, K., Torok, L., Marian, B., Ellinger, A., and Hermann, R. S. (2000) Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J. Cell Sci. 113, 1189-1198 (Pubitemid 30229536)
53. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514
54. Tanito, M., Masutani, H., Kim, Y. C., Nishikawa, M., Ohira, A., and Yodoi, J. (2005) Sulforaphane induces thioredoxin through the antioxidant-responsive element and attenuates retinal light damage in mice. Invest. Ophthalmol. Vis. Sci. 46, 979-987 (Pubitemid 41321036)
55. Neve, E. P., and Ingelman-Sundberg, M. (2008) Intracellular transport and localization of microsomal cytochrome P450. Anal. Bioanal. Chem. 392, 1075-1084
56. Gonzalez, F. J. (2005) Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat. Res. 569, 101-110
57. Zangar, R. C., Davydov, D. R., and Verma, S. (2004) Mechanisms that regulate production of reactive oxygen species by cytochrome P450. Toxicol. Appl. Pharmacol. 199, 316-331 (Pubitemid 39208731)
58. Penn, J. S., Naash, M. I., and Anderson, R. E. (1987) Effect of light history on retinal antioxidants and light damage susceptibility in the rat. Exp. Eye Res. 44, 779-788 (Pubitemid 17113218)
59. Tanito, M., Nishiyama, A., Tanaka, T., Masutani, H., Nakamura, H., Yodoi, J., and Ohira, A. (2002) Change of redox status and modulation by thiol replenishment in retinal photooxidative damage. Invest. Ophthalmol. Vis. Sci. 43, 2392-2400 (Pubitemid 34700673)
60. Jung, H., and Remé, C. (1994) Light-evoked arachidonic acid release in the retina: illuminance/duration dependence and the effects of quinacrine, mellitin and lithium. Light-evoked arachidonic acid release. Graefes Arch. Clin. Exp. Ophthalmol. 232, 167-175 (Pubitemid 24091737)
61. Kolko, M., Christoffersen, N. R., Barreiro, S. G., and Bazan, N. G. (2004) Expression and location of mRNAs encoding multiple forms of secretory phospholipase A2 in the rat retina. J. Neurosci. Res. 77, 517-524 (Pubitemid 39007003)
62. Rzigalinski, B. A., Willoughby, K. A., Hoffman, S. W., Falck, J. R., and Ellis, E. F. (1999) Calcium influx factor, further evidence it is 5,6-epoxyeico-satrienoic acid. J. Biol. Chem. 274, 175-182 (Pubitemid 29035046)
63. Berridge, M. J., Lipp, P., and Bootman, M. D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21
64. i regulation in apoptosis, oncosis, and necrosis. Biochim. Biophys. Acta 1313, 173-178
65. Mancy, A., Dijols, S., Poli, S., Guengerich, P., and Mansuy, D. (1996) Interaction of sulfaphenazole derivatives with human liver cytochromes P450 2C: molecular origin of the specific inhibitory effects of sulfaphenazole on CYP 2C9 and consequences for the substrate binding site topology of CYP 2C9. Biochemistry 35, 16205-16212
66. Krishnamoorthy, R. R., Crawford, M. J., Chaturvedi, M. M., Jain, S. K., Aggarwal, B. B., Al-Ubaidi, M. R., and Agarwal, N. (1999) Photo-oxidative stress down-modulates the activity of nuclear factor-κB via involvement of caspase-1, leading to apoptosis of photoreceptor cells. J. Biol. Chem. 274, 3734-3743 (Pubitemid 29077221)
67. Daikh, B. E., Lasker, J. M., Raucy, J. L., and Koop, D. R. (1994) Regio- and stereoselective epoxidation of arachidonic acid by human cytochromes P450 2C8 and 2C9. J. Pharmacol. Exp. Ther. 271, 1427-1433 (Pubitemid 24382654)
68. Wang, H., Zhao, Y., Bradbury, J. A., Graves, J. P., Foley, J., Blaisdell, J. A., Goldstein, J. A., and Zeldin, D. C. (2004) Cloning, expression, and characterization of three new mouse cytochrome P450 enzymes and partial characterization of their fatty acid oxidation activities. Mol. Pharmacol. 65, 1148-1158 (Pubitemid 38543486)
69. Luo, G., Zeldin, D. C., Blaisdell, J. A., Hodgson, E., and Goldstein, J. A. (1998) Cloning and expression of murine CYP2Cs and their ability to metabolize arachidonic acid. Arch. Biochem. Biophys. 357, 45-57 (Pubitemid 28402584)
70. Michaelis, U. R., Falck, J. R., Schmidt, R., Busse, R., and Fleming, I. (2005) Cytochrome P4502C9-derived epoxyeicosatrienoic acids induce the expression of cyclooxygenase-2 in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 25, 321-326 (Pubitemid 40189152)
71. Caro, A. A., and Cederbaum, A. I. (2006) Role of cytochrome P450 in phospholipase A2- and arachidonic acid-mediated cytotoxicity. Free Radic. Biol. Med. 40, 364-375 (Pubitemid 43139672)
72. 2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ. Res. 97, 908-915 (Pubitemid 41552676)
73. 2+ signaling and hyperpolarization in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 27, 2612-2618
74. Spector, A. A., Fang, X., Snyder, G. D., and Weintraub, N. L. (2004) Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog. Lipid Res. 43, 55-90 (Pubitemid 37433867)
75. Dumlao, D. S., Buczynski, M. W., Norris, P. C., Harkewicz, R., and Dennis, E. A. (2011) High-throughput lipidomic analysis of fatty acid derived eicosanoids and N-acylethanolamines. Biochim. Biophys. Acta 1811, 724-736
76. Krönke, G., Katzenbeisser, J., Uderhardt, S., Zaiss, M. M., Scholtysek, C., Schabbauer, G., Zarbock, A., Koenders, M. I., Axmann, R., Zwerina, J., Baenckler, H. W., van den Berg, W., Voll, R. E., Kühn, H., Joosten, L. A., and Schett, G. (2009) 12/15-Lipoxygenase counteracts inflammation and tissue damage in arthritis. J. Immunol. 183, 3383-3389
77. Tang, D. G., Chen, Y. Q., Honn, K. V. (1996) Arachidonate lipoxygenases as essential regulators of cell survival and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 93, 5241-5246 (Pubitemid 26159433)
78. Arnold, C., Markovic, M., Blossey, K., Wallukat, G., Fischer, R., Dechend, R., Konkel, A., von Schacky, C., Luft, F. C., Muller, D. N., Rothe, M., and Schunck, W. H. (2010) Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of ω-3 fatty acids. J. Biol. Chem. 285, 32720-32733
79. Fer, M., Dréano, Y., Lucas, D., Corcos, L., Salaün J. P., Berthou, F., and Amet, Y. (2008) Metabolism of eicosapentaenoic and docosahexaenoic acids by recombinant human cytochromes P450. Arch. Biochem. Biophys. 471, 116-125
80. Bazan, N. G., Calandria, J. M., and Serhan, C. N. (2010) Rescue and repair during photoreceptor cell renewal mediated by docosahexaenoic acid-derived neuroprotectin D1. J. Lipid Res. 51, 2018-2031
81. Hong, S., Gronert, K., Devchand, P.R., Moussignac, R. L., and Serhan, C. N. (2003) Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J. Biol. Chem. 278, 14677-14687 (Pubitemid 36799790)
82. Mukherjee, P. K., Marcheselli, V. L., Serhan, C. N., and Bazan, N. G. (2004) Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 101, 8491-8496 (Pubitemid 38736602)
83. Qian, L., Zolfaghari, R., and Ross, A. C. (2010) Liver-specific cytochrome P450 CYP2C22 is a direct target of retinoic acid and a retinoic acid-metabolizing enzyme in rat liver. J. Lipid Res. 51, 1781-1792
84. Marill, J., Cresteil, T., Lanotte, M., and Chabot, G. G. (2000) Identification of human cytochrome P450s involved in the formation of all-trans-retinoic acid principal metabolites. Mol. Pharmacol. 58, 1341-1348
85. de Lera, A. R., Bourguet, W., Altucci, L., and Gronemeyer, H. (2007) Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat. Rev. Drug Discov. 6, 811-820 (Pubitemid 47504872)
86. Schug, T. T., Berry, D. C., Shaw, N. S., Travis, S. N., and Noy, N. (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129, 723-733 (Pubitemid 46802374)
87. McCaffery, P., Mey, J., and Dräger, U. C. (1996) Light-mediated retinoic acid production. Proc. Natl. Acad. Sci. U.S.A. 93, 12570-12574 (Pubitemid 26367185)
88. Maeda, A., Golczak, M., Maeda, T., and Palczewski, K. (2009) Limited roles of Rdh8, Rdh12, and Abca4 in all-trans-retinal clearance in mouse retina. Invest. Ophthalmol. Vis. Sci. 50, 5435-5443
89. Sparrow, J. R., Fishkin, N., Zhou, J., Cai, B., Jang, Y. P., Krane, S., Itagaki, Y., and Nakanishi, K. (2003) A2E, a byproduct of the visual cycle. Vision Res. 43, 2983-2990 (Pubitemid 37377610)
90. Williams, P. A., Cosme, J., Ward, A., Angove, H. C., Matak Vinković, D., and Jhoti, H. (2003) Crystal structure of human cytochrome P450 2C9 with bound warfarin. Nature 424, 464-468