Rod outer segment retinol formation is independent of Abca4, arrestin, rhodopsin kinase, and rhodopsin palmitylation

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 6, 2011, Pages 3483-3491

  Blakeley, Lorie R ^a   Chen, Chunhe ^a   Chen, Ching Kang ^b   Chen, Jeannie ^c   Crouch, Rosalie K ^a   Travis, Gabriel H ^d   Koutalos, Yiannis ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A4; RETINA S ANTIGEN; RETINAL; RETINOL; RHODOPSIN; RHODOPSIN KINASE; UNCLASSIFIED DRUG; ABCA4 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME KINETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOUSE; NONBIOLOGICAL MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA ROD; RETINA ROD OUTER SEGMENT; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; LIPOYLATION; METABOLISM; MOUSE MUTANT; SPECTROFLUOROMETRY;

ANIMALS; ARRESTIN; ATP-BINDING CASSETTE TRANSPORTERS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; G-PROTEIN-COUPLED RECEPTOR KINASE 1; LIPOYLATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RHODOPSIN; ROD CELL OUTER SEGMENT; SPECTROMETRY, FLUORESCENCE; VITAMIN A;

EID: 80051716538     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6694     Document Type: Article

References (61)

1. Ebrey T, Koutalos Y. Vertebrate photoreceptors. Prog Retin Eye Res. 2001;20:49-94.
2. Palczewski K. G protein-coupled receptor rhodopsin. Annu Rev Biochem. 2006;75:743-767.
3. Fain GL, Matthews HR, Cornwall MC, Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev. 2001;81:117-151.
4. Burns ME, Arshavsky VY. Beyond counting photons: trials and trends in vertebrate visual transduction. Neuron. 2005;48:387-401.
5. Saari JC. Biochemistry of visual pigment regeneration: the Friedenwald lecture. Invest Ophthalmol Vis Sci. 2000;41:337-348.
6. Lamb TD, Pugh EN, Jr. Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res. 2004;23:307-380.
7. Travis GH, Golczak M, Moise AR, Palczewski K. Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu Rev Pharmacol Toxicol. 2007;47:469-512.
8. Palczewski K, Jager S, Buczylko J, et al. Rod outer segment retinol dehydrogenase: substrate specificity and role in phototransduction. Biochemistry. 1994;33:13741-13750.
9. Futterman S, Hendrickson A, Bishop PE, Rollins MH, Vacano E. Metabolism of glucose and reduction of retinaldehyde in retinal photoreceptors. J Neurochem. 1970;17:149-156.
10. Okajima TI, Pepperberg DR, Ripps H, Wiggert B, Chader GJ. Interphotoreceptor retinoid-binding protein: role in delivery of retinol to the pigment epithelium. Exp Eye Res. 1989;49:629-644.
11. Qtaishat NM, Wiggert B, Pepperberg DR. Interphotoreceptor retinoid-binding protein (IRBP) promotes the release of all-trans retinol from the isolated retina following rhodopsin bleaching illumination. Exp Eye Res. 2005;81:455-463.
12. Bernstein PS, Law WC, Rando RR. Isomerization of all-trans-retinoids to 11-cis-retinoids in vitro. Proc Natl Acad Sci U S A. 1987; 84:1849-1853.
13. Liu J, Itagaki Y, Ben-Shabat S, Nakanishi K, Sparrow JR. The biosynthesis of A2E, a fluorophore of aging retina, involves the formation of the precursor, A2-PE, in the photoreceptor outer segment membrane. J Biol Chem. 2000;275:29354-29360.
14. Delmelle M. Retinal sensitized photodynamic damage to liposomes. Photochem Photobiol. 1978;28:357-360.
15. Krasnovsky AA Jr, Kagan VE. Photosensitization and quenching of singlet oxygen by pigments and lipids of photoreceptor cells of the retina. FEBS Lett. 1979;108:152-154.
16. Sommer ME, Smith WC, Farrens DL. Dynamics of arrestin-rhodopsin interactions: arrestin and retinal release are directly linked events. J Biol Chem. 2005;280:6861-6871.
17. Hofmann KP, Pulvermuller A, Buczylko J, Van Hooser P, Palczewski K. The role of arrestin and retinoids in the regeneration pathway of rhodopsin. J Biol Chem. 1992;267:15701-15706.
18. Sachs K, Maretzki D, Meyer CK, Hofmann KP. Diffusible ligand all-trans-retinal activates opsin via a palmitoylation-dependent mechanism. J Biol Chem. 2000;275:6189-6194.
19. Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell. 1999;98:13-23.
20. Sun H, Molday RS, Nathans J. Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATPbinding cassette transporter responsible for Stargardt disease. J Biol Chem. 1999;274:8269-8281.
21. Beharry S, Zhong M, Molday, RS. N.-retinylidene-phosphatidylethanolamine is the preferred retinoid substrate for the photoreceptor-specific ABC transporter ABCA4 (ABCR). J Biol Chem. 2004;279:53972-53979.
22. Stone EM, Webster AR, Vandenburgh K, et al. Allelic variation in ABCR associated with Stargardt disease but not age-related macular degeneration. Nat Genet. 1998;20:328-329.
23. Allikmets R, Singh N, Sun H, et al. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet. 1997;15:236-246.
24. Yamamoto S, Sippel KC, Berson EL, Dryja TP. Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat Genet. 1997;15:175-178.
25. Fuchs S, Nakazawa M, Maw M, Tamai M, Oguchi Y, Gal A. A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat Genet. 1995;10:360-362.
26. Chen CK, Burns ME, Spencer M, et al. Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci U S A. 1999;96:3718-3722.
27. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, Chen J. Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature. 1997;389:505-509.
28. Wang Z, Wen XH, Ablonczy Z, Crouch RK, Makino CL, Lem J. Enhanced shutoff of phototransduction in transgenic mice expressing palmitoylation-deficient rhodopsin. J Biol Chem. 2005; 280:24293-24300.
29. Chen C, Blakeley LR, Koutalos Y. Formation of all-trans retinol after visual pigment bleaching in mouse photoreceptors. Invest Ophthalmol Vis Sci. 2009;50:3589-3595.
30. Fung BK, Hurley JB, Stryer L. Flow of information in the lighttriggered cyclic nucleotide cascade of vision. Proc Natl Acad Sci U S A. 1981;78:152-156.
31. Farrens DL, Khorana HG. Structure and function in rhodopsin: measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy. J Biol Chem. 1995;270:5073-5076.
32. Wu Q, Blakeley LR, Cornwall MC, Crouch RK, Wiggert BN, Koutalos Y. Interphotoreceptor retinoid-binding protein is the physio-logically relevant carrier that removes retinol from rod photoreceptor outer segments. Biochemistry. 2007;46:8669-8679.
33. Wenzel A, Reme CE, Williams TP, Hafezi F, Grimm C. The Rpe65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci. 2001;21:53-58.
34. Lyubarsky AL, Savchenko AB, Morocco SB, Daniele LL, Redmond TM, Pugh EN,. Jr. Mole quantity of RPE65 and its productivity in the generation of 11-cis-retinal from retinyl esters in the living mouse eye. Biochemistry. 2005;44:9880-9888.
35. Tsybovsky Y, Molday RS, Palczewski K. The ATP-binding cassette transporter ABCA4: structural and functional properties and role in retinal disease. Adv Exp Med Biol 703:105-125.
36. Imai H, Kuwayama S, Onishi A, Morizumi T, Chisaka O, Shichida Y. Molecular properties of rod and cone visual pigments from purified chicken cone pigments to mouse rhodopsin in situ. Photochem Photobiol Sci. 2005;4:667-674.
37. Chen J, Simon MI, Matthes MT, Yasumura D, LaVail MM. Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest Ophthalmol Vis Sci. 1999;40:2978-2982.
38. Saari JC, Nawrot M, Kennedy BN, et al. Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron. 2001;29:739-748.
39. Lem J, Krasnoperova NV, Calvert PD, et al. Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci U S A. 1999;96:736-741.
40. Matschinsky FM. Quantitative histochemistry of nicotinamide adenine nucleotides in retina of monkey and rabbit. J Neurochem. 1968;15:643-657.
41. Mata NL, Weng J, Travis GH. Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc Natl Acad Sci U S A. 2000;97:7154-7159.
42. Wu Y, Fishkin NE, Pande A, Pande J, Sparrow JR. Novel lipofuscin bisretinoids prominent in human retina and in a model of recessive Stargardt disease. J Biol Chem. 2009;284:20155-20166.
43. Kim SR, Jang YP, Jockusch S, Fishkin NE, Turro NJ, Sparrow JR. The all-trans-retinal dimer series of lipofuscin pigments in retinal pigment epithelial cells in a recessive Stargardt disease model. Proc Natl Acad Sci U S A. 2007;104:19273-19278.
44. Jager S, Palczewski K, Hofmann KP. Opsin/all-trans-retinal complex activates transducin by different mechanisms than photolyzed rhodopsin. Biochemistry. 1996;35:2901-2908.
45. Surya A, Knox BE. Enhancement of opsin activity by all-transretinal. Exp Eye Res. 1998;66:599-603.
46. Tsina E, Chen C, Koutalos Y, et al. Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors. J Gen Physiol. 2004;124:429-443.
47. Pawar AS, Qtaishat NM, Little DM, Pepperberg DR. Recovery of rod photoresponses in ABCR-deficient mice. Invest Ophthalmol Vis Sci. 2008;49:2743-2755.
48. Philp NJ, Chang W, Long K. Light-stimulated protein movement in rod photoreceptor cells of the rat retina. FEBS Lett. 1987;225:127-132.
49. Mangini NJ, Pepperberg DR. Immunolocalization of 48K in rod photoreceptors. Light and ATP increase OS labeling. Invest Ophthalmol Vis Sci. 1988;29:1221-1234.
50. Whelan JP, McGinnis JF. Light-dependent subcellular movement of photoreceptor proteins. J Neurosci Res. 1988;20:263-270.
51. Broekhuyse RM, Tolhuizen EF, Janssen AP, Winkens HJ. Light induced shift and binding of S-antigen in retinal rods. Curr Eye Res. 1985;4:613-618.
52. Strissel KJ, Sokolov M, Trieu LH, Arshavsky VY. Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J Neurosci. 2006;26: 1146-1153.
53. Chen C, Koutalos Y. Rapid formation of all-trans retinol after bleaching in frog and mouse rod photoreceptor outer segments. Photochem Photobiol Sci.
54. Heck M, Schadel SA, Maretzki D, et al. Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II. J Biol Chem. 2003;278:3162-3169.
55. Zimmermann K, Ritter E, Bartl FJ, Hofmann KP, Heck M. Interaction with transducin depletes metarhodopsin III: a regulated retinal storage in visual signal transduction? J Biol Chem. 2004;279: 48112-48119.
56. Park PS, Sapra KT, Jastrzebska B, et al. Modulation of molecular interactions and function by rhodopsin palmitylation. Biochemistry. 2009;48:4294-4304.
57. Maeda A, Maeda T, Golczak M, et al. Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J Biol Chem. 2009;284: 15173-15183.
58. Hao W, Wenzel A, Obin MS, et al. Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet. 2002; 32:254-260.
59. Maeda A, Okano K, Park PS, et al. Palmitoylation stabilizes unliganded rod opsin. Proc Natl Acad Sci U S A. 107:8428-8433.
60. Ala-Laurila P, Kolesnikov AV, Crouch RK, et al. Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology. J Gen Physiol. 2006;128:153-169.
61. Kolesnikov AV, Ala-Laurila P, Shukolyukov SA, et al. Visual cycle and its metabolic support in gecko photoreceptors. Vision Res. 2007;47:363-374.