Genomic deletion of CNGB3 is identical by descent in multiple canine breeds and causes achromatopsia

BMC Genetics

Volumn 14, Issue , 2013, Pages

  Yeh, Connie Y ^a,b   Goldstein, Orly ^c   Kukekova, Anna V ^c,d   Holley, Debbie ^e   Knollinger, Amy M ^f   Huson, Heather J ^g   Pearce Kelling, Susan E ^h   Acland, Gregory M ^c   Komáromy, András M ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Department of Molecular Biology and Genetics   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e Willow Creek Pet Center   (United States)

^f Eye Care For Animals   (United States)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

^h OptiGen   (United States)

Author keywords

Achromatopsia; Alaskan malamute; Alaskan sled dog; Australian shepherd; CNGB3; Cone degeneration; Day blindness; Identical by descent; Siberian husky

Indexed keywords

GENOMIC DNA;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME ANALYSIS; CNGB3 GENE; COLOR BLINDNESS; CONTROLLED STUDY; DNA DETERMINATION; DOG; GENE; GENE DELETION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ANALYSIS; GENETIC SCREENING; GENOTYPE; HAPLOTYPE; MALE; NONHUMAN; PHENOTYPE; VISUAL ACUITY; WILD TYPE;

ANIMALS; BREEDING; COLOR VISION DEFECTS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DNA MUTATIONAL ANALYSIS; DOG DISEASES; DOGS; FOUNDER EFFECT; GENOTYPE; LINKAGE DISEQUILIBRIUM; PHENOTYPE; SEQUENCE DELETION;

CANIS FAMILIARIS;

EID: 84876997127     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-14-27     Document Type: Article

References (45)

1. Michaelides M, Hunt DM, Moore AT. The cone dysfunction syndromes. Br J Ophthalmol 2004, 88:291-297. 10.1136/bjo.2003.027102, 1771989, 14736794.
2. Thiadens AA, den Hollander AI, Roosing S, Nabuurs SB, Zekveld-Vroon RC, Collin RW, De Baere E, Koenekoop RK, van Schooneveld MJ, Strom TM. Homozygosity mapping reveals PDE6C mutations in patients with early-onset cone photoreceptor disorders. Am J Hum Genet 2009, 85:240-247. 10.1016/j.ajhg.2009.06.016, 2725240, 19615668.
3. Kohl S, Coppieters F, Meire F, Schaich S, Roosing S, Brennenstuhl C, Bolz S, van Genderen MM, Riemslag FC, . European Retinal Disease Consortium A nonsense mutation in PDE6H causes autosomal-recessive incomplete achromatopsia. Am J Hum Genet 2012, 91:527-532. 10.1016/j.ajhg.2012.07.006, 3511981, 22901948, European Retinal Disease Consortium.
4. Kohl S, Baumann B, Rosenberg T, Kellner U, Lorenz B, Vadala M, Jacobson SG, Wissinger B. Mutations in the cone photoreceptor G-protein alpha-subunit gene GNAT2 in patients with achromatopsia. Am J Hum Genet 2002, 71:422-425. 10.1086/341835, 379175, 12077706.
5. Aligianis IA, Forshew T, Johnson S, Michaelides M, Johnson CA, Trembath RC, Hunt DM, Moore AT, Maher ER. Mapping of a novel locus for achromatopsia (ACHM4) to 1p and identification of a germline mutation in the alpha subunit of cone transducin (GNAT2). J Med Genet 2002, 39:656-660. 10.1136/jmg.39.9.656, 1735242, 12205108.
6. Kohl S, Marx T, Giddings I, Jagle H, Jacobson SG, Apfelstedt-Sylla E, Zrenner E, Sharpe LT, Wissinger B. Total colourblindness is caused by mutations in the gene encoding the alpha-subunit of the cone photoreceptor cGMP-gated cation channel. Nat Genet 1998, 19:257-259. 10.1038/935, 9662398.
7. Sundin OH, Yang JM, Li Y, Zhu D, Hurd JN, Mitchell TN, Silva ED, Maumenee IH. Genetic basis of total colourblindness among the Pingelapese islanders. Nat Genet 2000, 25:289-293. 10.1038/77162, 10888875.
8. Kohl S, Baumann B, Broghammer M, Jagle H, Sieving P, Kellner U, Spegal R, Anastasi M, Zrenner E, Sharpe LT. Mutations in the CNGB3 gene encoding the beta-subunit of the cone photoreceptor cGMP-gated channel are responsible for achromatopsia (ACHM3) linked to chromosome 8q21. Hum Mol Genet 2000, 9:2107-2116. 10.1093/hmg/9.14.2107, 10958649.
9. Kohl S, Varsanyi B, Antunes GA, Baumann B, Hoyng CB, Jagle H, Rosenberg T, Kellner U, Lorenz B, Salati R. CNGB3 mutations account for 50% of all cases with autosomal recessive achromatopsia. Eur J Hum Genet 2005, 13:302-308. 10.1038/sj.ejhg.5201269, 15657609.
10. Varsanyi B, Wissinger B, Kohl S, Koeppen K, Farkas A. Clinical and genetic features of Hungarian achromatopsia patients. Mol Vis 2005, 11:996-1001.
11. Wiszniewski W, Lewis RA, Lupski JR. Achromatopsia: the CNGB3 p.T383fsX mutation results from a founder effect and is responsible for the visual phenotype in the original report of uniparental disomy 14. Hum Genet 2007, 121:433-439. 10.1007/s00439-006-0314-y, 17265047.
12. Thiadens AA, Slingerland NW, Roosing S, van Schooneveld MJ, van Lith-Verhoeven JJ, van Moll-Ramirez N, van den Born LI, Hoyng CB, Cremers FP, Klaver CC. Genetic etiology and clinical consequences of complete and incomplete achromatopsia. Ophthalmology 2009, 116:1984-1989. 10.1016/j.ophtha.2009.03.053, 19592100.
13. Sidjanin DJ, Lowe JK, McElwee JL, Milne BS, Phippen TM, Sargan DR, Aguirre GD, Acland GM, Ostrander EA. Canine CNGB3 mutations establish cone degeneration as orthologous to the human achromatopsia locus ACHM3. Hum Mol Genet 2002, 11:1823-1833. 10.1093/hmg/11.16.1823, 12140185.
14. Komaromy AM, Alexander JJ, Rowlan JS, Garcia MM, Chiodo VA, Kaya A, Tanaka JC, Acland GM, Hauswirth WW, Aguirre GD. Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 2010, 19:2581-2593. 10.1093/hmg/ddq136, 2883338, 20378608.
15. Aguirre GD, Rubin LF. The electroretinogram in dogs with inherited cone degeneration. Invest Ophthalmol 1975, 14:840-847.
16. Aguirre GD, Rubin LF. Pathology of hemeralopia in the Alaskan malamute dog. Invest Ophthalmol 1974, 13:231-235.
17. Rubin LF. Hemeralopia in Alaskan Malamute pups. J Am Vet Med Assoc 1971, 158:1699-1701.
18. Rubin LF. Clinical features of hemeralopia in the adult Alaskan malamute. J Am Vet Med Assoc 1971, 158:1696-1698.
19. Long KO, Aguirre GD. The cone matrix sheath in the normal and diseased retina: cytochemical and biochemical studies of peanut agglutinin-binding proteins in cone and rod-cone degeneration. Exp Eye Res 1991, 52:699-713. 10.1016/0014-4835(91)90022-7, 1855544.
20. Parker HG, Kim LV, Sutter NB, Carlson S, Lorentzen TD, Malek TB, Johnson GS, DeFrance HB, Ostrander EA, Kruglyak L. Genetic structure of the purebred domestic dog. Science 2004, 304:1160-1164. 10.1126/science.1097406, 15155949.
21. Vonholdt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 2010, 464:898-902. 10.1038/nature08837, 3494089, 20237475.
22. Grozdanic SD, Matic M, Sakaguchi DS, Kardon RH. Evaluation of retinal status using chromatic pupil light reflex activity in healthy and diseased canine eyes. Invest Ophthalmol Vis Sci 2007, 48:5178-5183. 10.1167/iovs.07-0249, 17962471.
23. Jacobs GH, Deegan JF, Crognale MA, Fenwick JA. Photopigments of dogs and foxes and their implications for canid vision. Vis Neurosci 1993, 10:173-180. 10.1017/S0952523800003291, 8424924.
24. Neitz J, Geist T, Jacobs GH. Color vision in the dog. Vis Neurosci 1989, 3:119-125. 10.1017/S0952523800004430, 2487095.
25. Nalefski EA, Falke JJ. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 1996, 5:2375-2390. 10.1002/pro.5560051201, 2143302, 8976547.
26. Rizo J, Sudhof TC. C2-domains, structure and function of a universal Ca2 + -binding domain. J Biol Chem 1998, 273:15879-15882. 10.1074/jbc.273.26.15879, 9632630.
27. Seddon JM, Hampson EC, Smith RI, Hughes IP. Genetic heterogeneity of day blindness in Alaskan Malamutes. Anim Genet 2006, 37:407-410. 10.1111/j.1365-2052.2006.01484.x, 16879359.
28. Goldstein O, Zangerl B, Pearce-Kelling S, Sidjanin DJ, Kijas JW, Felix J, Acland GM, Aguirre GD. Linkage disequilibrium mapping in domestic dog breeds narrows the progressive rod-cone degeneration interval and identifies ancestral disease-transmitting chromosome. Genomics 2006, 88:541-550. 10.1016/j.ygeno.2006.05.013, 16859891.
29. van de Sluis B, Peter AT, Wijmenga C. Indirect molecular diagnosis of copper toxicosis in Bedlington terriers is complicated by haplotype diversity. J Hered 2003, 94:256-259. 10.1093/jhered/esg030, 12816967.
30. Clark LA, Wahl JM, Steiner JM, Zhou W, Ji W, Famula TR, Williams DA, Murphy KE. Linkage analysis and gene expression profile of pancreatic acinar atrophy in the German Shepherd Dog. Mamm Genome 2005, 16:955-962. 10.1007/s00335-005-0076-1, 16341675.
31. Farias FH, Johnson GS, Taylor JF, Giuliano E, Katz ML, Sanders DN, Schnabel RD, McKay SD, Khan S, Gharahkhani P. An ADAMTS17 splice donor site mutation in dogs with primary lens luxation. Invest Ophthalmol Vis Sci 2010, 51:4716-4721. 10.1167/iovs.09-5142, 20375329.
32. Gould D, Pettitt L, McLaughlin B, Holmes N, Forman O, Thomas A, Ahonen S, Lohi H, O'Leary C, Sargan D. ADAMTS17 mutation associated with primary lens luxation is widespread among breeds. Vet Ophthalmol 2011, 14:378-384. 10.1111/j.1463-5224.2011.00892.x, 22050825.
33. Huson HJ, Parker HG, Runstadler J, Ostrander EA. A genetic dissection of breed composition and performance enhancement in the Alaskan sled dog. BMC Genet 2010, 11:71. 2920855, 20649949.
34. Parker HG, Kukekova AV, Akey DT, Goldstein O, Kirkness EF, Baysac KC, Mosher DS, Aguirre GD, Acland GM, Ostrander EA. Breed relationships facilitate fine-mapping studies: a 7.8-kb deletion cosegregates with Collie eye anomaly across multiple dog breeds. Genome Res 2007, 17:1562-1571. 10.1101/gr.6772807, 2045139, 17916641.
35. Neff MW, Robertson KR, Wong AK, Safra N, Broman KW, Slatkin M, Mealey KL, Pedersen NC. Breed distribution and history of canine mdr1-1Delta, a pharmacogenetic mutation that marks the emergence of breeds from the collie lineage. Proc Natl Acad Sci U S A 2004, 101:11725-11730. 10.1073/pnas.0402374101, 511012, 15289602.
36. American College of Veterinary Ophthalmologists Genetics Committee Ocular Disorders Presumed to be Inherited in Purebred Dogs 2010, Meridian, ID: American College of Veterinary Ophthalmologists, 5, American College of Veterinary Ophthalmologists Genetics Committee.
37. Stanley RG, Acland GM, Vingrys A, Hardman C, Turner A, Smith REI, Hughes I. Day blindness in Alaskan malamutes in Australia: Clinical and electroretinographic findings. Proceedings of the 29th Annual Meeting of the American College of Veterinary Ophthalmologists: 21-24 October 1998; Seattle, WA 1998, 22.
38. Ding XQ, Harry CS, Umino Y, Matveev AV, Fliesler SJ, Barlow RB. Impaired cone function and cone degeneration resulting from CNGB3 deficiency: down-regulation of CNGA3 biosynthesis as a potential mechanism. Hum Mol Genet 2009, 18:4770-4780. 10.1093/hmg/ddp440, 2778372, 19767295.
39. Shamir MH, Ofri R, Bor A, Brenner O, Reicher S, Obolensky A, Averbukh E, Banin E, Gootwine E. A novel day blindness in sheep: epidemiological, behavioural, electrophysiological and histopathological studies. Vet J 2010, 185:130-137. 10.1016/j.tvjl.2009.05.029, 19546015.
40. Reicher S, Seroussi E, Gootwine E. A mutation in gene CNGA3 is associated with day blindness in sheep. Genomics 2010, 95:101-104. 10.1016/j.ygeno.2009.10.003, 19874885.
41. Pang JJ, Deng WT, Dai X, Lei B, Everhart D, Umino Y, Li J, Zhang K, Mao S, Boye SL. AAV-mediated cone rescue in a naturally occurring mouse model of CNGA3-achromatopsia. PLoS One 2012, 7:e35250. 10.1371/journal.pone.0035250, 3324465, 22509403.
42. Chang B, Grau T, Dangel S, Hurd R, Jurklies B, Sener EC, Andreasson S, Dollfus H, Baumann B, Bolz S. A homologous genetic basis of the murine cpfl1 mutant and human achromatopsia linked to mutations in the PDE6C gene. Proc Natl Acad Sci U S A 2009, 106:19581-19586. 10.1073/pnas.0907720106, 2780790, 19887631.
43. Chang B, Dacey MS, Hawes NL, Hitchcock PF, Milam AH, Atmaca-Sonmez P, Nusinowitz S, Heckenlively JR. Cone photoreceptor function loss-3, a novel mouse model of achromatopsia due to a mutation in Gnat2. Invest Ophthalmol Vis Sci 2006, 47:5017-5021. 10.1167/iovs.05-1468, 17065522.
44. Alexander JJ, Umino Y, Everhart D, Chang B, Min SH, Li Q, Timmers AM, Hawes NL, Pang JJ, Barlow RB. Restoration of cone vision in a mouse model of achromatopsia. Nat Med 2007, 13:685-687. 10.1038/nm1596, 17515894.
45. Garcia MM, Ying GS, Cocores CA, Tanaka JC, Komaromy AM. Evaluation of a behavioral method for objective vision testing and identification of achromatopsia in dogs. Am J Vet Res 2010, 71:97-102. 10.2460/ajvr.71.1.97, 2814178, 20043788.