A large animal model for CNGB1 autosomal recessive retinitis pigmentosa

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Winkler, Paige A ^a   Ekenstedt, Kari J ^b   Occelli, Laurence M ^a   Frattaroli, Anton V ^a   Bartoe, Joshua T ^a   Venta, Patrick J ^a,c   Petersen Jones, Simon M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN RIVER FALLS   (United States)

^c Department of Animal and Food Sciences University of Wisconsin River Falls ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; PEPTIDES AND PROTEINS; PROTEIN CNGA1; PROTEIN CNGB1; UNCLASSIFIED DRUG; CNGA1 PROTEIN, HUMAN; CNGB1 PROTEIN, HUMAN; CYCLIC NUCLEOTIDE GATED CHANNEL; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CARBOXY TERMINAL SEQUENCE; CNGB1 GENE; CONTROLLED STUDY; DISEASE MODEL; DOG BREED; EXON; FEMALE; FRAMESHIFT MUTATION; GENE DELETION; GENE INSERTION; GENE MAPPING; GENE SEQUENCE; GENETIC IDENTIFICATION; GENOMICS; HAPLOTYPE; HOMOZYGOSITY; HUMAN; IMMUNOHISTOCHEMISTRY; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPILLON DOG; PHENOTYPE; PROGRESSIVE RETINAL ATROPHY; RETINA DISEASE; RETINITIS PIGMENTOSA; SINGLE NUCLEOTIDE POLYMORPHISM; STOP CODON; ANIMAL; DOG; GENE EXPRESSION; GENETICS; INDEL MUTATION; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEIC ACID DATABASE; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; RECESSIVE GENE; RETINA ROD OUTER SEGMENT; SEQUENCE HOMOLOGY;

ANIMALIA; CANIS FAMILIARIS;

ANIMALS; BASE SEQUENCE; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DATABASES, NUCLEIC ACID; DISEASE MODELS, ANIMAL; DOGS; EXONS; FEMALE; GENE EXPRESSION; GENES, RECESSIVE; HUMANS; INDEL MUTATION; MICE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RETINITIS PIGMENTOSA; RNA, MESSENGER; ROD CELL OUTER SEGMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84898608640     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072229     Document Type: Article

References (68)

1. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368: 1795-1809.
2. Maubaret CG, Vaclavik V, Mukhopadhyay R, Waseem NH, Churchill A, et al. (2011) Autosomal dominant retinitis pigmentosa with intrafamilial variability and incomplete penetrance in two families carrying mutations in PRPF8. Invest Ophthalmol Vis Sci 52: 9304-9309.
3. Berson EL, Rosner B, Sandberg MA, Weigel-DiFranco C, Dryja TP (1991) Ocular findings in patients with autosomal dominant retinitis pigmentosa and rhodopsin, proline-347-leucine. Am J Ophthalmol 111: 614-623.
4. Whitley RD (1988) Focusing on eye disorders among purebred dogs. Veterinary Medicine 83: 50-63.
5. Petersen-Jones SM (1998) Animal models of human retinal dystrophies. Eye 12 (Pt 3b): 566-570.
6. Aguirre GD, Acland GM (2006) Models, mutants, and man: searching for unique phenotypes and genes in the dog model of inherited retinal degeneration. In: Ostrander EA, Giger U, Lindblad-Toh K, editors. The dog and its genome. Cold Spring Harbor: Cold Spring harbor Laboratory Press. 291-326.
7. Suber ML, Pittler SJ, Quin N, Wright GC, Holcombe N, et al. (1993) Irish setter dogs affected with rod-cone dysplasia contain a nonsense mutation in the rod cGMP phosphodiesterase beta-subunit gene. Proc Natl Acad Sci U S A 90: 3968-3972.
8. Clements PJ, Gregory CY, Peterson-Jones SM, Sargan DR, Bhattacharya SS (1993) Confirmation of the rod cGMP phosphodiesterase beta subunit (PDE beta) nonsense mutation in affected rcd-1 Irish setters in the UK and development of a diagnostic test. Curr Eye Res 12: 861-866.
9. Petersen-Jones SM, Entz DD, Sargan DR (1999) cGMP phosphodiesterase-a mutation causes progressive retinal atrophy in the Cardigan Welsh corgi dog. Invest Ophthalmol Vis Sci 40: 1637-1644.
10. Dekomien G, Runte M, Godde R, Epplen JT (2000) Generalized progressive retinal atrophy of Sloughi dogs is due to an 8-bp insertion in exon 21 of the PDE6B gene. Cytogenet Cell Genet 90: 261-267.
11. Zhu L, Jang GF, Jastrzebska B, Filipek S, Pearce-Kelling SE, et al. (2004) A naturally occurring mutation of the opsin gene (T4R) in dogs affects glycosylation and stability of the G protein-coupled receptor. J Biol Chem 279: 53828-53839.
12. Kukekova AV, Goldstein O, Johnson JL, Richardson MA, Pearce-Kelling SE, et al. (2009) Canine RD3 mutation establishes rod-cone dysplasia type 2 (rcd2) as ortholog of human and murine rd3. Mamm Genome 20: 109-123.
13. Downs LM, Bell JS, Freeman J, Hartley C, Hayward LJ, et al. (2012) Late-onset progressive retinal atrophy in the Gordon and Irish Setter breeds is associated with a frameshift mutation in C2orf71. Anim Genet 44: 169-177.
14. Goldstein O, Kukekova AV, Aguirre GD, Acland GM (2010) Exonic SINE insertion in STK38L causes canine early retinal degeneration (erd). Genomics 96: 362-368.
15. Zangerl B, Goldstein O, Philp AR, Lindauer SJ, Pearce-Kelling SE, et al. (2006) Identical mutation in a novel retinal gene causes progressive rod-cone degeneration in dogs and retinitis pigmentosa in humans. Genomics 88: 551-563.
16. Downs LM, Wallin-Hakansson B, Boursnell M, Marklund S, Hedhammar A, et al. (2011) A frameshift mutation in golden retriever dogs with progressive retinal atrophy endorses SLC4A3 as a candidate gene for human retinal degenerations. PLoS One 6: e21452.
17. Mowat FM, Petersen-Jones SM, Williamson H, Williams DL, Luthert PJ, et al. (2008) Topographical characterization of cone photoreceptors and the area centralis of the canine retina. Mol Vis 14: 2518-2527.
18. 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: 245-262.
19. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS, et al. (2001) Gene therapy restores vision in a canine model of childhood blindness. Nat genet 28: 92-95.
20. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, et al. (2008) Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
21. Maguire AM, Simonelli F, Pierce EA, Pugh EN, Jr., Mingozzi F, et al. (2008) Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240-2248.
22. Cideciyan AV, Hauswirth WW, Aleman TS, Kaushal S, Schwartz SB, 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: 999-1004.
23. Acland GM, Aguirre GD, Bennett J, Aleman TS, Cideciyan AV, et al. (2005) Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol Ther 12: 1072-1082.
24. Narfström K, Katz ML, Bragadottir R, Seeliger M, Boulanger A, et al. (2003) Functional and structural recovery of the retina after gene therapy in the RPE65 null mutation dog. Invest Ophthalmol Vis Sci 44: 1663-1672.
25. Jacobson SG, Acland GM, Aguirre GD, Aleman TS, Schwartz SB, et al. (2006) Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol Ther 13: 1074-1084.
26. Annear MJ, Bartoe JT, Barker SE, Smith AJ, Curran PG, et al. (2011) Gene therapy in the second eye of RPE65-deficient dogs improves retinal function. Gene Ther 18: 53-61.
27. Gearhart PM, Gearhart C, Thompson DA, Petersen-Jones SM (2010) Improvement of visual performance with intravitreal administration of 9-cis-retinal in Rpe65-mutant dogs. Arch Ophthalmol 128: 1442-1448.
28. Beltran WA, Cideciyan AV, Lewin AS, Iwabe S, Khanna H, et al. (2012) Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human X-linked retinitis pigmentosa. Proc Natl Acad Sci U S A 109: 2132-2137.
29. Komaromy AM, Alexander JJ, Rowlan JS, Garcia MM, Chiodo VA, et al. (2010) Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 19: 2581-2593.
30. Mowat FM, Bartoe JT, Bruewer A, Dinculescu A, Boye SL, et al. (2012) Evaluation Of Rod Photoreceptor Function And Preservation Following Retinal Gene Therapy In The PDE6A Mutant Dog. ARVO Meeting Abstracts 53: 1928.
31. Petit L, Lheriteau E, Weber M, Le Meur G, Deschamps JY, et al. (2012) Restoration of vision in the pde6beta-deficient dog, a large animal model of rod-cone dystrophy. Mol Ther 20: 2019-2030.
32. Håkanson N, Narfström K (1995) Progressive retinal atrophy in papillon dogs in Sweden: A clinical survey. Vet Comp Ophthalmol 5: 83-87.
33. Narfström K, Ekesten B (1998) Electroretinographic evaluation of Papillons with and without hereditary retinal degeneration. Am J Vet Res 59: 221-226.
34. Narfström K, Wrigstad A (1999) Clinical, electrophysiological and morphological changes in a case of hereditary retinal degeneration in the Papillon dog. Vet Ophthalmol 2: 67-74.
35. Gum GG, Gelatt KC, Samuelson DA (1984) Maturation of the retina of the canine neonate as determined by electroretinography and histology. Am J Vet Res 45: 1166-1171.
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575.
37. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006.
38. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
39. Colville CA, Molday RS (1996) Primary structure and expression of the human beta-subunit and related proteins of the rod photoreceptor cGMP-gated channel. J Biol Chem 271: 32968-32974.
40. Ardell MD, Bedsole DL, Schoborg RV, Pittler SJ (2000) Genomic organization of the human rod photoreceptor cGMP-gated cation channel beta-subunit gene. Gene 245: 311-318.
41. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82: 769-824.
42. Sautter A, Zong X, Hofmann F, Biel M (1998) An isoform of the rod photoreceptor cyclic nucleotide-gated channel beta subunit expressed in olfactory neurons. Proc Natl Acad Sci U S A 95: 4696-4701.
43. Chen TY, Peng YW, Dhallan RS, Ahamed B, Reed RR, et al. (1993) A new subunit of the cyclic nucleotide-gated cation channel in retinal rods. Nature 362: 764-767.
44. Wiesner B, Weiner J, Middendorff R, Hagen V, Kaupp UB, et al. (1998) Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J Cell Biol 142: 473-484.
45. Huttl S, Michalakis S, Seeliger M, Luo DG, Acar N, et al. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J Neurosci 25: 130-138.
46. Zhang Y, Molday LL, Molday RS, Sarfare SS, Woodruff ML, et al. (2009) Knockout of GARPs and the beta-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J Cell Sci 122: 1192-1200.
47. Sugimoto Y, Yatsunami K, Tsujimoto M, Khorana HG, Ichikawa A (1991) The amino acid sequence of a glutamic acid-rich protein from bovine retina as deduced from the cDNA sequence. Proc Natl Acad Sci U S A 88: 3116-3119.
48. Zheng J, Trudeau MC, Zagotta WN (2002) Rod cyclic nucleotide-gated channels have a stoichiometry of three CNGA1 subunits and one CNGB1 subunit. Neuron 36: 891-896.
49. Zhong H, Molday LL, Molday RS, Yau KW (2002) The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420: 193-198.
50. Weitz D, Ficek N, Kremmer E, Bauer PJ, Kaupp UB (2002) Subunit stoichiometry of the CNG channel of rod photoreceptors. Neuron 36: 881-889.
51. Shuart NG, Haitin Y, Camp SS, Black KD, Zagotta WN (2011) Molecular mechanism for 3:1 subunit stoichiometry of rod cyclic nucleotide-gated ion channels. Nat Commun 2: 457.
52. Chen TY, Illing M, Molday LL, Hsu YT, Yau KW, et al. (1994) Subunit 2 (or beta) of retinal rod cGMP-gated cation channel is a component of the 240-kDa channel-associated protein and mediates Ca(2+)-calmodulin modulation. Proc Natl Acad Sci U S A 91: 11757-11761.
53. Kaupp UB, Niidome T, Tanabe T, Terada S, Bönigk W, et al. (1989) Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342: 762-766.
54. Pentia DC, Hosier S, Cote RH (2006) The glutamic acid-rich protein-2 (GARP2) is a high affinity rod photoreceptor phosphodiesterase (PDE6)-binding protein that modulates its catalytic properties. J Biol Chem 281: 5500-5505.
55. Ritter LM, Khattree N, Tam B, Moritz OL, Schmitz F, et al. (2011) In situ visualization of protein interactions in sensory neurons: glutamic acid-rich proteins (GARPs) play differential roles for photoreceptor outer segment scaffolding. J Neurosci 31: 11231-11243.
56. Michalakis S, Zong X, Becirovic E, Hammelmann V, Wein T, et al. (2011) The glutamic acid-rich protein is a gating inhibitor of cyclic nucleotide-gated channels. J Neurosci 31: 133-141.
57. Trudeau MC, Zagotta WN (2002) An intersubunit interaction regulates trafficking of rod cyclic nucleotide-gated channels and is disrupted in an inherited form of blindness. Neuron 34: 197-207.
58. Zheng J, Zagotta WN (2004) Stoichiometry and assembly of olfactory cyclic nucleotide-gated channels. Neuron 42: 411-421.
59. Michalakis S, Reisert J, Geiger H, Wetzel C, Zong X, et al. (2006) Loss of CNGB1 protein leads to olfactory dysfunction and subciliary cyclic nucleotide-gated channel trapping. J Biol Chem 281: 35156-35166.
60. Bareil C, Hamel CP, Delague V, Arnaud B, Demaille J, et al. (2001) Segregation of a mutation in CNGB1 encoding the beta-subunit of the rod cGMP-gated channel in a family with autosomal recessive retinitis pigmentosa. Hum Genet 108: 328-334.
61. Simpson DA, Clark GR, Alexander S, Silvestri G, Willoughby CE (2011) Molecular diagnosis for heterogeneous genetic diseases with targeted high-throughput DNA sequencing applied to retinitis pigmentosa. J Med Genet 48: 145-151.
62. Kondo H, Qin M, Mizota A, Kondo M, Hayashi H, et al. (2004) A homozygosity-based search for mutations in patients with autosomal recessive retinitis pigmentosa, using microsatellite markers. Invest Ophthalmol Vis Sci 45: 4433-4439.
63. Becirovic E, Nakova K, Hammelmann V, Hennel R, Biel M, et al. (2010) The retinitis pigmentosa mutation c.3444+1G.A in CNGB1 results in skipping of exon 32. PLoS One 5: e8969.
64. Koch S, Sothilingam V, Garcia Garrido M, Tanimoto N, Becirovic E, et al. (2012) Gene therapy restores vision and delays degeneration in the CNGB1(2/2) mouse model of retinitis pigmentosa. Hum Mol Genet 21: 4486-4496.
65. Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78: 629-644.
66. Mowat FM, Breuwer AR, Bartoe JT, Annear MJ, Zhang Z, et al. (2012) RPE65 gene therapy slows cone loss in Rpe65-deficient dogs. Gene Ther DOI:10.1038/gt.2012.63.
67. Cook NJ, Molday LL, Reid D, Kaupp UB, Molday RS (1989) The cGMP-gated channel of bovine rod photoreceptors is localized exclusively in the plasma membrane. J Biol Chem 264: 6996-6999.
68. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.