Genetic defects of GDF6 in the zebrafish out of sight mutant and in human eye developmental anomalies

BMC Genetics

Volumn 11, Issue , 2010, Pages

  den Hollander, Anneke I ^a,b   Biyanwila, Janisha ^a   Kovach, Peter ^a   Bardakjian, Tanya ^c   Traboulsi, Elias I ^d   Ragge, Nicola K ^e,f   Schneider, Adele ^c   Malicki, Jarema ^a  

^a TUFTS UNIVERSITY   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ALBERT EINSTEIN MEDICAL CENTER   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; EMBRYO; EYE MALFORMATION; GDF6 GENE; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC DISORDER; HUMAN; INTERNEURON; MICROPHTHALMIA; NERVOUS SYSTEM DEVELOPMENT; OUT OF SIGHT GENE; PHENOTYPE; RETINA; ZEBRA FISH; ANIMAL; CELL PROLIFERATION; CHROMOSOME MAP; EYE; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR CLONING; MUTATION; ORGAN SIZE; PRENATAL DEVELOPMENT;

DANIO RERIO; VERTEBRATA;

GDF6A PROTEIN, ZEBRAFISH; GROWTH DIFFERENTIATION FACTOR 6; ZEBRAFISH PROTEIN;

AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CHROMOSOME MAPPING; CLONING, MOLECULAR; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH DIFFERENTIATION FACTOR 6; HUMANS; MICROPHTHALMOS; MUTATION; ORGAN SIZE; PHENOTYPE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 78149299827     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-11-102     Document Type: Article

References (54)

1. Lowry RB, Kohut R, Sibbald B, Rouleau J. Anophthalmia and microphthalmia in the Alberta Congenital Anomalies Surveillance System. Can J Ophthalmol 2005, 40:38-44.
2. Morrison D, FitzPatrick D, Hanson I, Williamson K, van H V, Fleck B, Jones I, Chalmers J, Campbell H. National study of microphthalmia, anophthalmia, and coloboma (MAC) in Scotland: investigation of genetic aetiology. J Med Genet 2002, 39:16-22. 10.1136/jmg.39.1.16, 1734963, 11826019.
3. Shaw GM, Carmichael SL, Yang W, Harris JA, Finnell RH, Lammer EJ. Epidemiologic characteristics of anophthalmia and bilateral microphthalmia among 2.5 million births in California, 1989-1997. Am J Med Genet A 2005, 137:36-40.
4. Gregory-Evans CY, Williams MJ, Halford S, Gregory-Evans K. Ocular coloboma: a reassessment in the age of molecular neuroscience. J Med Genet 2004, 41:881-891. 10.1136/jmg.2004.025494, 1735648, 15591273.
5. Verma AS, Fitzpatrick DR. Anophthalmia and microphthalmia. Orphanet J Rare Dis 2007, 2:47. 10.1186/1750-1172-2-47, 2246098, 18039390.
6. Fantes J, Ragge NK, Lynch SA, McGill NI, Collin JR, Howard-Peebles PN, Hayward C, Vivian AJ, Williamson K, van HV, Fitzpatrick DR. Mutations in SOX2 cause anophthalmia. Nat Genet 2003, 33:461-463. 10.1038/ng1120, 12612584.
7. Ferda PE, Ploder LA, Yu JJ, Arici K, Horsford DJ, Rutherford A, Bapat B, Cox DW, Duncan AM, Kalnins VI, Kocak-Altintas A, Sowden JC, Traboulsi E, Sarfarazi M, McInnes RR. Human microphthalmia associated with mutations in the retinal homeobox gene CHX10. Nat Genet 2000, 25:397-401. 10.1038/78071, 10932181.
8. Glaser T, Jepeal L, Edwards JG, Young SR, Favor J, Maas RL. PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat Genet 1994, 7:463-471. 10.1038/ng0894-463, 7951315.
9. Ragge NK, Brown AG, Poloschek CM, Lorenz B, Henderson RA, Clarke MP, Russell-Eggitt I, Fielder A, Gerrelli D, Martinez-Barbera JP, Ruddle P, Hurst J, Collin JR, Salt A, Cooper ST, Thompson PJ, Sisodiya SM, Williamson KA, Fitzpatrick DR, van H V, Hanson IM. Heterozygous mutations of OTX2 cause severe ocular malformations. Am J Hum Genet 2005, 76:1008-1022. 10.1086/430721, 1196439, 15846561.
10. Voronina VA, Kozhemyakina EA, O'Kernick CM, Kahn ND, Wenger SL, Linberg JV, Schneider AS, Mathers PH. Mutations in the human RAX homeobox gene in a patient with anophthalmia and sclerocornea. Hum Mol Genet 2004, 13:315-322. 10.1093/hmg/ddh025, 14662654.
11. Bakrania P, Efthymiou M, Klein JC, Salt A, Bunyan DJ, Wyatt A, Ponting CP, Martin A, Williams S, Lindley V, Gilmore J, Restori M, Robson AG, Neveu MM, Holder GE, Collin JR, Robinson DO, Farndon P, Johansen-Berg H, Gerrelli D, Ragge NK. Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways. Am J Hum Genet 2008, 82:304-319. 10.1016/j.ajhg.2007.09.023, 2427285, 18252212.
12. Ye M, Berry-Wynne KM, sai-Coakwell M, Sundaresan P, Footz T, French CR, Abitbol M, Fleisch VC, Corbett N, Allison WT, Drummond G, Walter MA, Underhill TM, Waskiewicz AJ, Lehmann OJ. Mutation of the bone morphogenetic protein GDF3 causes ocular and skeletal anomalies. Hum Mol Genet 2010, 19:287-298. 10.1093/hmg/ddp496, 19864492.
13. Asai-Coakwell M, French CR, Berry KM, Ye M, Koss R, Somerville M, Mueller R, van H V, Waskiewicz AJ, Lehmann OJ. GDF6, a novel locus for a spectrum of ocular developmental anomalies. Am J Hum Genet 2007, 80:306-315. 10.1086/511280, 1785352, 17236135.
14. Asai-Coakwell M, French CR, Ye M, Garcha K, Bigot K, Perera AG, Staehling-Hampton K, Mema SC, Chanda B, Mushegian A, Bamforth S, Doschak MR, Li G, Dobbs MB, Giampietro PF, Brooks BP, Vijayalakshmi P, Sauve Y, Abitbol M, Sundaresan P, van H V, Pourquie O, Underhill TM, Waskiewicz AJ, Lehmann OJ. Incomplete penetrance and phenotypic variability characterize Gdf6-attributable oculo-skeletal phenotypes. Hum Mol Genet 2009, 18:1110-1121. 10.1093/hmg/ddp008, 19129173.
15. Gonzalez-Rodriguez J, Pelcastre EL, Tovilla-Canales JL, Garcia-Ortiz JE, mato-Almanza M, Villanueva-Mendoza C, Espinosa-Mattar Z, Zenteno JC. Mutational screening of CHX10, GDF6, OTX2, RAX and SOX2 genes in 50 unrelated microphthalmia-anophthalmia-coloboma (MAC) spectrum cases. Br J Ophthalmol 2010, 94:1100-1104. 10.1136/bjo.2009.173500, 20494911.
16. Hogan BL. Bone morphogenetic proteins in development. Curr Opin Genet Dev 1996, 6:432-438. 10.1016/S0959-437X(96)80064-5, 8791534.
17. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. Novel regulators of bone formation: molecular clones and activities. Science 1988, 242:1528-1534. 10.1126/science.3201241, 3201241.
18. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008, 1782:197-228.
19. Xiao YT, Xiang LX, Shao JZ. Bone morphogenetic protein. Biochem Biophys Res Commun 2007, 362:550-553. 10.1016/j.bbrc.2007.08.045, 17719560.
20. Reddi AH. BMPs: from bone morphogenetic proteins to body morphogenetic proteins. Cytokine Growth Factor Rev 2005, 16:249-250. 10.1016/j.cytogfr.2005.04.003, 15949967.
21. Tassabehji M, Fang ZM, Hilton EN, McGaughran J, Zhao Z, de Bock CE, Howard E, Malass M, Donnai D, Diwan A, Manson FD, Murrell D, Clarke RA. Mutations in GDF6 are associated with vertebral segmentation defects in Klippel-Feil syndrome. Hum Mutat 2008, 29:1017-1027. 10.1002/humu.20741, 18425797.
22. Hanel ML, Hensey C. Eye and neural defects associated with loss of GDF6. BMC Dev Biol 2006, 6:43. 10.1186/1471-213X-6-43, 1609107, 17010201.
23. Settle SH, Rountree RB, Sinha A, Thacker A, Higgins K, Kingsley DM. Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 2003, 254:116-130. 10.1016/S0012-1606(02)00022-2, 12606286.
24. Gosse NJ, Baier H. An essential role for Radar (Gdf6a) in inducing dorsal fate in the zebrafish retina. Proc Natl Acad Sci USA 2009, 106:2236-2241. 10.1073/pnas.0803202106, 2650138, 19164594.
25. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, Belak J, Boggs C. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 1996, 123:37-46.
26. Malicki J, Neuhauss SC, Schier AF, Solnica-Krezel L, Stemple DL, Stainier DY, Abdelilah S, Zwartkruis F, Rangini Z, Driever W. Mutations affecting development of the zebrafish retina. Development 1996, 123:263-273.
27. Pedersen AG, Nielsen H. Neural network prediction of translation initiation sites in eukaryotes: perspectives for EST and genome analysis. Proc Int Conf Intell Syst Mol Biol 1997, 5:226-233.
28. Peterson RE, Fadool JM, McClintock J, Linser PJ. Muller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J Comp Neurol 2001, 429:530-540. 10.1002/1096-9861(20010122)429:4<530::AID-CNE2>3.0.CO;2-C, 11135233.
29. Avanesov A, Dahm R, Sewell WF, Malicki JJ. Mutations that affect the survival of selected amacrine cell subpopulations define a new class of genetic defects in the vertebrate retina. Dev Biol 2005, 285:138-155. 10.1016/j.ydbio.2005.06.009, 16231865.
30. Ekstrom P, Johansson K. Differentiation of ganglion cells and amacrine cells in the rat retina: correlation with expression of HuC/D and GAP-43 proteins. Brain Res Dev Brain Res 2003, 145:1-8. 10.1016/S0165-3806(03)00170-6, 14519488.
31. Macdonald R, Wilson SW. Distribution of Pax6 protein during eye development suggests discrete roles in proliferative and differentiated visual cells. Dev Genes Evol 1997, 206:363-369.
32. Larison KD, Bremiller R. Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 1990, 109:567-576.
33. Schmitt EA, Dowling JE. Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish, Danio rerio. J Comp Neurol 1996, 371:222-234. 10.1002/(SICI)1096-9861(19960722)371:2<222::AID-CNE3>3.0.CO;2-4, 8835728.
34. Hidalgo A, ffrench-Constant C. The control of cell number during central nervous system development in flies and mice. Mech Dev 2003, 120:1311-1325. 10.1016/j.mod.2003.06.004, 14623440.
35. Leevers SJ, McNeill H. Controlling the size of organs and organisms. Curr Opin Cell Biol 2005, 17:604-609. 10.1016/j.ceb.2005.09.008, 16226450.
36. Hu M, Easter SS. Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev Biol 1999, 207:309-321. 10.1006/dbio.1998.9031, 10068465.
37. Xiao T, Roeser T, Staub W, Baier H. A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 2005, 132:2955-2967. 10.1242/dev.01861, 15930106.
38. Dahm R, Schonthaler HB, Soehn AS, van MJ, Vrensen GF. Development and adult morphology of the eye lens in the zebrafish. Exp Eye Res 2007, 85:74-89. 10.1016/j.exer.2007.02.015, 17467692.
39. Lang RA. Apoptosis in mammalian eye development: lens morphogenesis, vascular regression and immune privilege. Cell Death Differ 1997, 4:12-20. 10.1038/sj.cdd.4400211, 16465205.
40. Allende ML, Amsterdam A, Becker T, Kawakami K, Gaiano N, Hopkins N. Insertional mutagenesis in zebrafish identifies two novel genes, pescadillo and dead eye, essential for embryonic development. Genes Dev 1996, 10:3141-3155. 10.1101/gad.10.24.3141, 8985183.
41. Fadool JM, Brockerhoff SE, Hyatt GA, Dowling JE. Mutations affecting eye morphology in the developing zebrafish (Danio rerio). Dev Genet 1997, 20:288-295. 10.1002/(SICI)1520-6408(1997)20:3<288::AID-DVG11>3.0.CO;2-4, 9216068.
42. Crosier PS, Kalev-Zylinska ML, Hall CJ, Flores MV, Horsfield JA, Crosier KE. Pathways in blood and vessel development revealed through zebrafish genetics. Int J Dev Biol 2002, 46:493-502.
43. Hall CJ, Flores MV, Davidson AJ, Crosier KE, Crosier PS. Radar is required for the establishment of vascular integrity in the zebrafish. Dev Biol 2002, 251:105-117. 10.1006/dbio.2002.0794, 12413901.
44. Ekker SC, Larson JD. Morphant technology in model developmental systems. Genesis 2001, 30:89-93. 10.1002/gene.1038, 11477681.
45. Omori Y, Malicki J. oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol 2006, 16:945-957. 10.1016/j.cub.2006.03.058, 16713951.
46. Tsujikawa M, Malicki J. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 2004, 42:703-716. 10.1016/S0896-6273(04)00268-5, 15182712.
47. Williams LA, Bhargav D, Diwan AD. Unveiling the bmp13 enigma: redundant morphogen or crucial regulator?. Int J Biol Sci 2008, 4:318-329. 2536705, 18797508.
48. Delot E, Kataoka H, Goutel C, Yan YL, Postlethwait J, Wittbrodt J, Rosa FM. The BMP-related protein radar: a maintenance factor for dorsal neuroectoderm cells?. Mech Dev 1999, 85:15-25. 10.1016/S0925-4773(99)00026-X, 10415343.
49. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310.
50. Malicki J, Jo H, Wei X, Hsiung M, Pujic Z. Analysis of gene function in the zebrafish retina. Methods 2002, 28:427-438. 10.1016/S1046-2023(02)00262-1, 12507461.
51. Malicki J. Development of the retina. Methods Cell Biol 1999, 59:273-299. full_text, 9891365.
52. Pujic Z, Malicki J. Mutation of the zebrafish glass onion locus causes early cell-nonautonomous loss of neuroepithelial integrity followed by severe neuronal patterning defects in the retina. Dev Biol 2001, 234:454-469. 10.1006/dbio.2001.0251, 11397013.
53. Avanesov A, Malicki J. Approaches to study neurogenesis in the zebrafish retina. Methods Cell Biol 2004, 76:333-384. full_text, 15602883.
54. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, Kelsh RN, Furutani-Seiki M, Vogelsang E, Beuchle D, Schach U, Fabian C, Nusslein-Volhard C. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 1996, 123:1-36.