Reprogramming of adult rod photoreceptors prevents retinal degeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 5, 2013, Pages 1732-1737

  Montana, Cynthia L ^a   Kolesnikov, Alexander V ^a   Shen, Susan Q ^a   Myers, Connie A ^a   Kefalov, Vladimir J ^a   Corbo, Joseph C ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Rd1; Rhodopsin; Transdifferentiation

Indexed keywords

NRL PROTEIN; PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DNA METHYLATION; DNA MODIFICATION; DOWN REGULATION; ELECTRORETINOGRAM; EPIGENETICS; GENE EXPRESSION; GENE FREQUENCY; GENE INACTIVATION; GENE MUTATION; MITOCHONDRION; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA CONE; RETINA DEGENERATION; RETINA ROD; RETINITIS PIGMENTOSA;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CPG ISLANDS; DNA METHYLATION; ELECTRORETINOGRAPHY; EYE PROTEINS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; RETINITIS PIGMENTOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN;

EID: 84873173426     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214387110     Document Type: Article

References (51)

1. Sohocki MM, et al. (2001) Prevalence of mutations causing retinitis pigmentosa and other inherited retinopathies. Hum Mutat 17(1):42-51. (Pubitemid 32054366)
2. Liu MM, Tuo J, Chan CC (2011) Gene therapy for ocular diseases. Br J Ophthalmol 95(5):604-612.
3. Cideciyan AV, et al. (2009) Human RPE65 gene therapy for Leber congenital amaurosis: Persistence of early visual improvements and safety at 1 year. Hum Gene Ther 20(9):999-1004.
4. Daiger SP, Rossiter BJF, Greenberg J, Christoffels A, Hide W (1998) RetNet, the Retinal Information Network. Available at https://sph.uth.edu/ RetNet/. Accessed August 10, 2012.
5. Montana CL, Corbo JC (2008) Inherited diseases of photoreceptors and prospects for gene therapy. Pharmacogenomics 9(3):335-347. (Pubitemid 351803936)
6. Farrar GJ, Kenna PF, Humphries P (2002) On the genetics of retinitis pigmentosa and on mutation: Independent approaches to therapeutic intervention. EMBO J 21(5):857-864. (Pubitemid 34206159)
7. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368(9549):1795-1809. (Pubitemid 44739028)
8. Komeima K, Rogers BS, Lu L, Campochiaro PA (2006) Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proc Natl Acad Sci USA 103(30):11300-11305. (Pubitemid 44159928)
9. Punzo C, Kornacker K, Cepko CL (2009) Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 12(1):44-52.
10. Miyamoto M, et al. (2010) A nonsense mutation in Gnat1, encoding the alpha subunit of rod transducin, in spontaneous mouse models of retinal dysfunction. Exp Eye Res 90(1):63-69.
11. Calvert PD, et al. (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci USA 97(25):13913-13918.
12. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA (2008) In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455(7213):627-632.
13. Izumikawa M, et al. (2005) Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 11(3):271-276. (Pubitemid 40460554)
14. Vierbuchen T, et al. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463(7284):1035-1041.
15. Yoo AS, et al. (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476(7359):228-231.
16. McAlear SD, Kraft TW, Gross AK (2010) 1 rhodopsin mutations in congenital night blindness. Adv Exp Med Biol 664:263-272.
17. Mears AJ, et al. (2001) Nrl is required for rod photoreceptor development. Nat Genet 29(4):447-452. (Pubitemid 34326696)
18. Daniele LL, et al. (2005) Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest Ophthalmol Vis Sci 46(6):2156-2167.
19. Roger JE, et al. (2012) Preservation of cone photoreceptors after a rapid yet transient degeneration and remodeling in cone-only Nrl-/-mouse retina. J Neurosci 32(2):528-541.
20. Carter-Dawson LD, LaVail MM, Sidman RL (1978) Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci 17(6):489-498. (Pubitemid 8357273)
21. Corbo JC, Myers CA, Lawrence KA, Jadhav AP, Cepko CL (2007) A typology of photoreceptor gene expression patterns in the mouse. Proc Natl Acad Sci USA 104(29):12069-12074. (Pubitemid 47185631)
22. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: A tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244(2):305-318. (Pubitemid 34450645)
23. Solovei I, et al. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137(2):356-368.
24. Corbo JC, Cepko CL (2005) A hybrid photoreceptor expressing both rod and cone genes in a mouse model of enhanced S-cone syndrome. PLoS Genet 1(2):e11.
25. Carter-Dawson LD, LaVail MM (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188(2):245-262. (Pubitemid 10193123)
26. Heikkinen H, Nymark S, Koskelainen A (2008) Mouse cone photoresponses obtained with electroretinogram from the isolated retina. Vision Res 48(2):264-272.
27. Wang JS, Kefalov VJ (2009) An alternative pathway mediates the mouse and human cone visual cycle. Curr Biol 19(19):1665-1669.
28. Kolesnikov AV, Kefalov VJ (2012) Transretinal ERG recordings from mouse retina: Rod and cone photoresponses. J Vis Exp 2012(61):61.
29. Chen J, Rattner A, Nathans J (2005) The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J Neurosci 25(1):118-129. (Pubitemid 40110772)
30. Chen J, Rattner A, Nathans J (2006) Effects of L1 retrotransposon insertion on transcript processing, localization and accumulation: Lessons from the retinal degeneration 7 mouse and implications for the genomic ecology of L1 elements. Hum Mol Genet 15(13):2146-2156. (Pubitemid 43923404)
31. Fruttiger M (2007) Development of the retinal vasculature. Angiogenesis 10(2):77-88. (Pubitemid 46440628)
32. Lem J, et al. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci USA 96(2):736-741. (Pubitemid 29061278)
33. Jaissle GB, et al. (2001) Evaluation of the rhodopsin knockout mouse as a model of pure cone function. Invest Ophthalmol Vis Sci 42(2):506-513. (Pubitemid 32121487)
34. Akimoto M, et al. (2006) Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors. Proc Natl Acad Sci USA 103(10):3890-3895. (Pubitemid 43376651)
35. Oh EC, et al. (2007) Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc Natl Acad Sci USA 104(5):1679-1684. (Pubitemid 46214650)
36. Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25(10):1010-1022.
37. Deng WT, et al. (2009) Functional interchangeability of rod and cone transducin alpha-subunits. Proc Natl Acad Sci USA 106(42):17681-17686.
38. Tachibanaki S, Tsushima S, Kawamura S (2001) Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses. Proc Natl Acad Sci USA 98(24):14044-14049. (Pubitemid 33116021)
39. Nikonov SS, et al. (2005) Photoreceptors of Nrl-/-mice coexpress functional S-and M-cone opsins having distinct inactivation mechanisms. J Gen Physiol 125(3):287-304. (Pubitemid 40388310)
40. Tachibanaki S, Arinobu D, Shimauchi-Matsukawa Y, Tsushima S, Kawamura S (2005) Highly effective phosphorylation by G protein-coupled receptor kinase 7 of lightactivated visual pigment in cones. Proc Natl Acad Sci USA 102(26):9329-9334. (Pubitemid 40923563)
41. Wada Y, Sugiyama J, Okano T, Fukada Y (2006) GRK1 and GRK7: Unique cellular distribution and widely different activities of opsin phosphorylation in the zebrafish rods and cones. J Neurochem 98(3):824-837. (Pubitemid 44051283)
42. Weiss ER, et al. (2001) Species-specific differences in expression of G-protein-coupled receptor kinase (GRK) 7 and GRK1 in mammalian cone photoreceptor cells: Implications for cone cell phototransduction. J Neurosci 21(23):9175-9184. (Pubitemid 33096861)
43. Zhang X, Wensel TG, Kraft TW (2003) GTPase regulators and photoresponses in cones of the eastern chipmunk. J Neurosci 23(4):1287-1297. (Pubitemid 36258907)
44. Jones GJ, Crouch RK, Wiggert B, Cornwall MC, Chader GJ (1989) Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photoreceptors. Proc Natl Acad Sci USA 86(23):9606-9610. (Pubitemid 20010477)
45. Wang JS, Estevez ME, Cornwall MC, Kefalov VJ (2009) Intra-retinal visual cycle required for rapid and complete cone dark adaptation. Nat Neurosci 12(3):295-302.
46. Mata NL, Radu RA, Clemmons RC, Travis GH (2002) Isomerization and oxidation of vitamin a in cone-dominant retinas: A novel pathway for visual-pigment regeneration in daylight. Neuron 36(1):69-80.
47. Wen R, et al. (2006) Regulation of rod phototransduction machinery by ciliary neurotrophic factor. J Neurosci 26(52):13523-13530. (Pubitemid 46026484)
48. Wen R, Tao W, Li Y, Sieving PA (2012) CNTF and retina. Prog Retin Eye Res 31(2):136-151.
49. Chen CM, Cepko CL (2000) Expression of Chx10 and Chx10-1 in the developing chicken retina. Mech Dev 90(2):293-297. (Pubitemid 30042937)
50. Kolesnikov AV, et al. (2011) G-protein betagamma-complex is crucial for efficient signal amplification in vision. J Neurosci 31(22):8067-8077.
51. Montana CL, et al. (2011) Transcriptional regulation of neural retina leucine zipper (Nrl), a photoreceptor cell fate determinant. J Biol Chem 286(42):36921-36931.