CRALBP supports the mammalian retinal visual cycle and cone vision

Journal of Clinical Investigation

Volumn 125, Issue 2, 2015, Pages 727-738

  Xue, Yunlu ^a,b   Shen, Susan Q ^b,c   Jui, Jonathan ^d   Rupp, Alan C ^e   Byrne, Leah C ^d   Hattar, Samer ^e   Flannery, John G ^d   Corbo, Joseph C ^c   Kefalov, Vladimir J ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b Division of Biological and Biomedical Sciences   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR RETINALDEHYDE BINDING PROTEIN; CONE OPSIN; M OPSIN; MELANOPSIN; RETINOID BINDING PROTEIN; UNCLASSIFIED DRUG; 11-CIS-RETINAL-BINDING PROTEIN; CARRIER PROTEIN; OPSIN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B WAVE; CONTROLLED STUDY; DARK ADAPTATION; DETERIORATION; GENE DELETION; LIGHT INTENSITY; MOUSE; MUELLER CELL; NONHUMAN; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUPIL REFLEX; RETINA; VISION; VISUAL IMPAIRMENT; ANIMAL; BLINDNESS; DEPENDOPARVOVIRUS; GENETIC TRANSDUCTION; GENETICS; KNOCKOUT MOUSE; MACROGLIA; METABOLISM; PATHOLOGY; PHYSIOLOGY; PIGMENT EPITHELIUM; PROTEIN TRANSPORT; RETINA CONE;

ANIMALS; BLINDNESS; CARRIER PROTEINS; DARK ADAPTATION; DEPENDOVIRUS; EPENDYMOGLIAL CELLS; MICE; MICE, KNOCKOUT; OPSINS; PROTEIN TRANSPORT; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL PIGMENT EPITHELIUM; TRANSDUCTION, GENETIC; VISION, OCULAR;

EID: 84963949815     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI79651     Document Type: Article

References (57)

1. Saari JC. Vitamin A metabolism in rod and cone visual cycles. Annu Rev Nutr. 2012;32:125-145.
2. Wang J-S, Kefalov VJ. The cone-specific visual cycle. Prog Retin Eye Res. 2011;30(2):115-128.
3. Mata NL, Radu RA, Clemmons RS, Travis GH. Isomerization and oxidation of vitamin a in cone-dominant retinas: a novel pathway for visual-pigment regeneration in daylight. Neuron. 2002;36(1):69-80.
4. Wang J-S, Estevez ME, Cornwall MC, Kefalov VJ. Intra-retinal visual cycle required for rapid and complete cone dark adaptation. Nat Neurosci. 2009;12(3):295-302.
5. Wang J-S, Kefalov VJ. An alternative pathway mediates the mouse and human cone visual cycle. Curr Biol. 2009;19(19):1665-1669.
6. Kolesnikov AV, Tang PH, Parker RO, Crouch RK, Kefalov VJ. The Mammalian cone visual cycle promotes rapid m/l-cone pigment regeneration independently of the interphotoreceptor retinoid-binding protein. J Neurosci. 2011;31(21):7900-7909.
7. Kaylor JJ, et al. Identification of DES1 as a vitamin A isomerase in Müller glial cells of the retina. Nat Chem Biol. 2013;9(1):30-36.
8. Kaylor JJ, et al. Identification of the 11-cis-specific retinyl-ester synthase in retinal Müller cells as multifunctional O-acyltransferase (MFAT). Proc Natl Acad Sci U S A. 2014;111(20):7302-7307.
9. Liu T, Jenwitheesuk E, Teller DC, Samudrala R. Structural insights into the cellular retinaldehydebinding protein (CRALBP). Proteins. 2005;61(2):412-422.
10. Fleisch VC, Schonthaler HB, Von Lintig J, Neuhauss SCF. Subfunctionalization of a retinoidbinding protein provides evidence for two parallel visual cycles in the cone-dominant zebrafish retina. J Neurosci. 2008;28(33):8208-8216.
11. Collery R, et al. Duplication and divergence of zebrafish CRALBP genes uncovers novel role for RPE- and Muller-CRALBP in cone vision. Invest Ophthalmol Vis Sci. 2008;49(9):3812-3820.
12. Babino D, Perkins BD, Kindermann A, Oberhauser V, Von Lintig J. The role of 11-cis-retinyl esters in vertebrate cone vision. FASEB J. 2015;29(1):216-226.
13. Maw MA, et al. Mutation of the gene encoding cellular retinaldehyde-binding protein in autosomal recessive retinitis pigmentosa. Nat Genet. 1997;17(2):198-200.
14. Burstedt MS, Sandgren O, Holmgren G, Forsman-Semb K. Bothnia dystrophy caused by mutations in the cellular retinaldehyde-binding protein gene (RLBP1) on chromosome 15q26. Invest Ophthalmol Vis Sci. 1999;40(5):995-1000.
15. Burstedt MS, et al. Ocular phenotype of bothnia dystrophy, an autosomal recessive retinitis pigmentosa associated with an R234W mutation in the RLBP1 gene. Arch Ophthalmol. 2001;119(2):260-267.
16. Burstedt MSI, Sandgren O, Golovleva I, Wachtmeister L. Retinal function in Bothnia dystrophy. An electrophysiological study. Vision Res. 2003;43(24):2559-2571.
17. Morimura H, Berson EL, Dryja TP. Recessive mutations in the RLBP1 gene encoding cellular retinaldehyde-binding protein in a form of retinitis punctata albescens. Invest Ophthalmol Vis Sci. 1999;40(5):1000-1004.
18. Naz S, et al. Mutations in RLBP1 associated with fundus albipunctatus in consanguineous Pakistani families. Br J Ophthalmol. 2011;95(7):1019-1024.
19. Katsanis N, et al. Fundus albipunctatus and retinitis punctata albescens in a pedigree with an R150Q mutation in RLBP1. Clin Genet. 2001;59(6):424-429.
20. Eichers ER, et al. Newfoundland rod-cone dystrophy, an early-onset retinal dystrophy, is caused by splice-junction mutations in RLBP1. Am J Hum Genet. 2002;70(4):955-964.
21. Thompson DA, Gal A. Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases. Prog Retin Eye Res. 2003;22(5):683-703.
22. Saari JC, et al. Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron. 2001;29(3):739-748.
23. Calvert PD, et al. Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci U S A. 2000;97(25):13913-13918.
24. Nikonov SS, Kholodenko R, Lem J, Pugh EN. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J Gen Physiol. 2006;127(4):359-374.
25. Keller C, Grimm C, Wenzel A, Hafezi F, Remé C. Protective effect of halothane anesthesia on retinal light damage: inhibition of metabolic rhodopsin regeneration. Invest Ophthalmol Vis Sci. 2001;42(2):476-480.
26. Ablonczy Z, et al. 11-cis-retinal reduces constitutive opsin phosphorylation and improves quantum catch in retinoid-deficient mouse rod photoreceptors. J Biol Chem. 2002;277(43):40491-40498.
27. Rohrer B, et al. Correlation of regenerable opsin with rod ERG signal in Rpe65-/-mice during development and aging. Invest Ophthalmol Vis Sci. 2003;44(1):310-315.
28. Dunn FA, Della Santina L, Parker ED, Wong ROL. Sensory experience shapes the development of the visual system's first synapse. Neuron. 2013;80(5):1159-1166.
29. Hattar S, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003;424(6944):76-81.
30. Wong K. Intrinsically photosensitive retinal ganglion cells (ipRGCs) depend on the retinal pigment epithelium (RPE) to regenerate melanopsin [abstract]. Invest Ophthalmol Vis Sci. 2013;54:400.
31. Xue T, et al. Melanopsin signalling in mammalian iris and retina. Nature. 2011;479(7371):67-73.
32. Lucas RJ, et al. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003;299(5604):245-247.
33. Tu DC, et al. Inner retinal photoreception independent of the visual retinoid cycle. Proc Natl Acad Sci U S A. 2006;103(27):10426-10431.
34. Goldstein EB. Cone pigment regeneration in the isolated frog retina. Vision Res. 1970;10(10):1065-1068.
35. Muniz A, et al. Evidence for two retinoid cycles in the cone-dominated chicken eye. Biochemistry. 2009;48(29):6854-6863.
36. Saari JC, Crabb JW. Focus on molecules: cellular retinaldehyde-binding protein (CRALBP). Exp Eye Res. 2005;81(3):245-246.
37. Nawrot M, et al. Cellular retinaldehyde-binding protein interacts with ERM-binding phosphoprotein 50 in retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2004;45(2):393-401.
38. Bonilha VL, et al. Support for a proposed retinoid-processing protein complex in apical retinal pigment epithelium. Exp Eye Res. 2004;79(3):419-422.
39. Jin M, et al. The role of interphotoreceptor retinoidbinding protein on the translocation of visual retinoids and function of cone photoreceptors. J Neurosci. 2009;29(5):1486-1495.
40. Parker RO, Fan J, Nickerson JM, Liou GI, Crouch RK. Normal cone function requires the interphotoreceptor retinoid binding protein. J Neurosci. 2009;29(14):4616-4621.
41. Redmond TM, et al. Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet. 1998;20(4):344-351.
42. Znoiko SL, et al. Downregulation of cone-specific gene expression and degeneration of cone photoreceptors in the Rpe65-/-mouse at early ages. Invest Ophthalmol Vis Sci. 2005;46(4):1473-1479.
43. Jacobson SG, et al. Human cone photoreceptor dependence on RPE65 isomerase. Proc Natl Acad Sci U S A. 2007;104(38):15123-15128.
44. Cottet S, et al. Biological characterization of gene response in Rpe65-/-mouse model of Leber's congenital amaurosis during progression of the disease. FASEB J. 2006;20(12):2036-2049.
45. Insinna C, et al. An S-opsin knock-in mouse (F81Y) reveals a role for the native ligand 11-cisretinal in cone opsin biosynthesis. J Neurosci. 2012;32(23):8094-8104.
46. Zhang H, et al. Trafficking of membrane-associated proteins to cone photoreceptor outer segments requires the chromophore 11-cis-retinal. J Neurosci. 2008;28(15):4008-4014.
47. Cunea A, Powner MB, Jeffery G. Death by color: differential cone loss in the aging mouse retina. Neurobiol. 2014;35(11):2584-2591.
48. Mattapallil MJ, et al. The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci. 2012;53(6):2921-2927.
49. Sundermeier TR, et al. DICER1 is essential for survival of postmitotic rod photoreceptor cells in mice. FASEB J. 2014;28(8):3780-3791.
50. Sundermeier TR, et al. R9AP overexpression alters phototransduction kinetics in iCre75 mice. Invest Ophthalmol Vis Sci. 2014;55(3):1339-1347.
51. Vinberg F, Kolesnikov AV, Kefalov VJ. Ex vivo ERG analysis of photoreceptors using an in vivo ERG system. Vision Res. 2014;101:108-117.
52. Pugh EN, Lamb TD. Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta. 1993;1141(2-3):111-149.
53. Saari JC, Nawrot M, Stenkamp RE, Teller DC, Garwin GG. Release of 11-cis-retinal from cellular retinaldehyde-binding protein by acidic lipids. Mol Vis. 2009;15:844-854.
54. Klimczak RR, Koerber JT, Dalkara D, Flannery JG, Schaffer DV. A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells. PLoS One. 2009;4(10):e7467.
55. Dalkara D, et al. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci Transl Med. 2013;5(189):189ra76.
56. Esumi N, Oshima Y, Li Y, Campochiaro PA, Zack DJ. Analysis of the VMD2 promoter and implication of E-box binding factors in its regulation. J Biol Chem. 2004;279(18):19064-19073.
57. Aurnhammer C, et al. Universal real-time PCR for the detection and quantification of adenoassociated virus serotype 2-derived inverted terminal repeat sequences. Hum Gene Ther. 2012;23(1):18-28.