A secreted WNT-ligand-binding domain of FZD5 generated by a frameshift mutation causes autosomal dominant coloboma

Human Molecular Genetics

Volumn 25, Issue 7, 2016, Pages 1382-1391

  Liu, Chunqiao ^a,b   Widen, Sonya A ^c   Williamson, Kathleen A ^d   Ratnapriya, Rinki ^a   Gerth Kahlert, Christina ^e   Rainger, Joe ^d   Alur, Ramakrishna P ^a   Strachan, Erin ^c   Manjunath, Souparnika H ^a   Balakrishnan, Archana ^a   Floyd, James A ^f   Li, Tiansen ^a   Waskiewicz, Andrew ^c   Brooks, Brian ^a   Lehmann, Ordan J ^c   FitzPatrick, David R ^d   Swaroop, Anand ^a,f  

^a NATIONAL EYE INSTITUTE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FRIZZLED PROTEIN; PROTEIN FZD5; UNCLASSIFIED DRUG; FZD5 PROTEIN, HUMAN; FZD5 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CASE REPORT; COLOBOMA; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; EXON; FEMALE; FRAMESHIFT MUTATION; HETEROZYGOTE; HUMAN; HUMAN CELL; LIGAND BINDING; MICROPHTHALMIA; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SECRETION; WNT SIGNALING PATHWAY; ANIMAL; DNA MUTATIONAL ANALYSIS; GENETICS; MALE; METABOLISM; MOUSE; PEDIGREE; ZEBRA FISH;

ANIMALS; DNA MUTATIONAL ANALYSIS; FEMALE; FRAMESHIFT MUTATION; FRIZZLED RECEPTORS; HUMANS; MALE; MICE; MICROPHTHALMOS; PEDIGREE; WNT SIGNALING PATHWAY; ZEBRAFISH;

EID: 84963746146     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw020     Document Type: Article

References (44)

1. Hornby, S.J., Gilbert, C.E., Rahi, J.K., Sil, A.K., Xiao, Y., Dandona, L. and Foster, A. (2000) Regional variation in blindness in children due to microphthalmos, anophthalmos and coloboma. Ophthalmic. Epidemiol., 7, 127-138.
2. Gregory-Evans, C.Y., Williams, M.J., Halford, S. and Gregory- Evans, K. (2004) Ocular coloboma: a reassessment in the age of molecular neuroscience. J. Med. Genet., 41, 881-891.
3. Williamson, K.A. and FitzPatrick, D.R. (2014) The genetic architecture of microphthalmia, anophthalmia and coloboma. Eur. J. Med. Genet., 57, 369-380.
4. Bakrania, P., Efthymiou, M., Klein, J.C., Salt, A., Bunyan, D.J., Wyatt, A., Ponting, C.P., Martin, A., Williams, S., Lindley, V. et al. (2008) Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways. Am. J. Hum. Genet., 82, 304-319.
5. Rainger, J., van Beusekom, E., Ramsay, J.K., McKie, L., Al-Gazali, L., Pallotta, R., Saponari, A., Branney, P., Fisher, M., Morrison, H. et al. (2011) Loss of the BMP antagonist, SMOC-1, causes ophthalmo-acromelic (Waardenburg anophthalmia) syndrome in humans and mice. PLoS. Genet., 7, e1002114.
6. Wyatt, A.W., Osborne, R.J., Stewart, H. and Ragge, N.K. (2010) Bone morphogenetic protein 7 (BMP7) mutations are associated with variable ocular, brain, ear, palate, and skeletal anomalies. Hum. Mutat., 31, 781-787.
7. Asai-Coakwell, M., French, C.R., Berry, K.M., Ye, M., Koss, R., Somerville, M., Mueller, R., van Heyningen, V., Waskiewicz, A.J. and Lehmann, O.J. (2007) GDF6, a novel locus for a spectrum of ocular developmental anomalies. Am. J. Hum. Genet., 80, 306-315.
8. Schimmenti, L.A., de la Cruz, J., Lewis, R.A., Karkera, J.D., Manligas, G.S., Roessler, E. and Muenke, M. (2003) Novel mutation in sonic hedgehog in non-syndromic colobomatous microphthalmia. Am. J. Med. Genet. A., 116A, 215-221.
9. Pasutto, F., Sticht, H., Hammersen, G., Gillessen-Kaesbach, G., Fitzpatrick, D.R., Nurnberg, G., Brasch, F., Schirmer-Zimmermann, H., Tolmie, J.L., Chitayat, D. et al. (2007) Mutations in STRA6 cause a broad spectrum of malformations including anophthalmia, congenital heart defects, diaphragmatic hernia, alveolar capillary dysplasia, lung hypoplasia, and mental retardation. Am. J. Hum. Genet., 80, 550-560.
10. Srour, M., Chitayat, D., Caron, V., Chassaing, N., Bitoun, P., Patry, L., Cordier, M.P., Capo-Chichi, J.M., Francannet, C., Calvas, P. et al. (2013) Recessive and dominant mutations in retinoic acid receptor beta in cases with microphthalmia and diaphragmatic hernia. Am. J. Hum. Genet., 93, 765-772.
11. Fares-Taie, L., Gerber, S., Chassaing, N., Clayton-Smith, J., Hanein, S., Silva, E., Serey, M., Serre, V., Gerard, X., Baumann, C. et al. (2013) ALDH1A3 mutations cause recessive anophthalmia and microphthalmia. Am. J. Hum. Genet., 92, 265-270.
12. Williamson, K.A., Rainger, J., Floyd, J.A., Ansari, M., Meynert, A., Aldridge, K.V., Rainger, J.K., Anderson, C.A., Moore, A.T., Hurles, M.E. et al. (2014) Heterozygous loss-of-function mutations in YAP1 cause both isolated and syndromic optic fissure closure defects. Am. J. Hum. Genet., 94, 295-302.
13. Ye, M., Berry-Wynne, K.M., Asai-Coakwell, M., Sundaresan, P., Footz, T., French, C.R., Abitbol, M., Fleisch, V.C., Corbett, N., Allison,W.T. et al. (2010) Mutation of the bone morphogenetic protein GDF3 causes ocular and skeletal anomalies. Hum. Mol. Genet., 19, 287-298.
14. Morcillo, J., Martinez-Morales, J.R., Trousse, F., Fermin, Y., Sowden, J.C. and Bovolenta, P. (2006) Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development, 133, 3179-3190.
15. Reis, L.M., Tyler, R.C., Schilter, K.F., Abdul-Rahman, O., Innis, J.W., Kozel, B.A., Schneider, A.S., Bardakjian, T.M., Lose, E.J., Martin, D.M. et al. (2011) BMP4 loss-of-function mutations in developmental eye disorders including SHORT syndrome. Hum. Genet., 130, 495-504.
16. Chen, Z.Y., Battinelli, E.M., Fielder, A., Bundey, S., Sims, K., Breakefield, X.O. and Craig, I.W. (1993) A mutation in the Norrie disease gene (NDP) associated with X-linked familial exudative vitreoretinopathy. Nat. Genet., 5, 180-183.
17. Nikopoulos, K., Venselaar, H., Collin, R.W., Riveiro-Alvarez, R., Boonstra, F.N., Hooymans, J.M., Mukhopadhyay, A., Shears, D., van Bers, M., de Wijs, I.J. et al. (2010) Overview of the mutation spectrum in familial exudative vitreoretinopathy and Norrie disease with identification of 21 novel variants in FZD4, LRP5, and NDP. Hum. Mutat., 31, 656-666.
18. Gong, Y., Slee, R.B., Fukai, N., Rawadi, G., Roman-Roman, S., Reginato, A.M., Wang, H., Cundy, T., Glorieux, F.H., Lev, D. et al. (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell, 107, 513-523.
19. Robitaille, J., MacDonald, M.L., Kaykas, A., Sheldahl, L.C., Zeisler, J., Dube, M.P., Zhang, L.H., Singaraja, R.R., Guernsey, D.L., Zheng, B. et al. (2002) Mutant frizzled-4 disrupts retinal angiogenesis in familial exudative vitreoretinopathy. Nat. Genet., 32, 326-330.
20. Toomes, C., Bottomley, H.M., Jackson, R.M., Towns, K.V., Scott, S., Mackey, D.A., Craig, J.E., Jiang, L., Yang, Z., Trembath, R. et al. (2004) Mutations in LRP5 or FZD4 underlie the common familial exudative vitreoretinopathy locus on chromosome 11q. Am. J. Hum. Genet., 74, 721-730.
21. Poulter, J.A., Davidson, A.E., Ali,M., Gilmour, D.F., Parry, D.A., Mintz-Hittner, H.A., Carr, I.M., Bottomley, H.M., Long, V.W., Downey, L.M. et al. (2012) Recessive mutations in TSPAN12 cause retinal dysplasia and severe familial exudative vitreoretinopathy (FEVR). Invest. Ophthalmol. Vis. Sci., 53, 2873-2879.
22. Cavodeassi, F., Carreira-Barbosa, F., Young, R.M., Concha,M.L., Allende, M.L., Houart, C., Tada, M. and Wilson, S.W. (2005) Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron, 47, 43-56.
23. Hagglund, A.C., Berghard, A. and Carlsson, L. (2013) Canonical Wnt/beta-catenin signalling is essential for optic cup formation. PLoS One, 8, e81158.
24. Lieven, O. and Ruther, U. (2011) The Dkk1 dose is critical for eye development. Dev. Biol., 355, 124-137.
25. Veien, E.S., Rosenthal, J.S., Kruse-Bend, R.C., Chien, C.B. and Dorsky, R.I. (2008) Canonical Wnt signaling is required for the maintenance of dorsal retinal identity. Development, 135, 4101-4111.
26. Holly, V.L., Widen, S.A., Famulski, J.K. and Waskiewicz, A.J. (2014) Sfrp1a and Sfrp5 function as positive regulators of Wnt and BMP signaling during early retinal development. Dev. Biol., 388, 192-204.
27. Liu, C. and Nathans, J. (2008) An essential role for frizzled 5 in mammalian ocular development. Development, 135, 3567-3576.
28. Borello, U., Buffa, V., Sonnino, C., Melchionna, R., Vivarelli, E. and Cossu, G. (1999) Differential expression of the Wnt putative receptors Frizzled during mouse somitogenesis. Mech. Dev., 89, 173-177.
29. Sumanas, S. and Ekker, S.C. (2001) Xenopus frizzled-5: a frizzled family member expressed exclusively in the neural retina of the developing eye. Mech. Dev., 103, 133-136.
30. Van Raay, T.J., Moore, K.B., Iordanova, I., Steele, M., Jamrich, M., Harris, W.A. and Vetter, M.L. (2005) Frizzled 5 signaling governs the neural potential of progenitors in the developing Xenopus retina. Neuron, 46, 23-36.
31. Burns, C.J., Zhang, J., Brown, E.C., Van Bibber, A.M., Van Es, J., Clevers, H., Ishikawa, T.O., Taketo, M.M., Vetter, M.L. and Fuhrmann, S. (2008) Investigation of Frizzled-5 during embryonic neural development in mouse. Dev. Dyn., 237, 1614-1626.
32. Liu, C., Bakeri, H., Li, T. and Swaroop, A. (2012) Regulation of retinal progenitor expansion by Frizzled receptors: implications for microphthalmia and retinal coloboma. Hum. Mol. Genet., 21, 1848-1860.
33. Zhou, C.J., Molotkov, A., Song, L., Li, Y., Pleasure, D.E., Pleasure, S.J. andWang, Y.Z. (2008) Ocular coloboma and dorsoventral neuroretinal patterning defects in Lrp6 mutant eyes. Dev. Dyn., 237, 3681-3689.
34. Carmon, K.S. and Loose, D.S. (2008) Secreted frizzled-related protein 4 regulates two Wnt7a signaling pathways and inhibits proliferation in endometrial cancer cells. Mol. Cancer. Res., 6, 1017-1028.
35. Carmon, K.S. and Loose, D.S. (2010) Development of a bioassay for detection of Wnt-binding affinities for individual frizzled receptors. Anal. Biochem., 401, 288-294.
36. Bodine, P.V., Zhao, W., Kharode, Y.P., Bex, F.J., Lambert, A.J., Goad, M.B., Gaur, T., Stein, G.S., Lian, J.B. and Komm, B.S. (2004) The Wnt antagonist secreted frizzled-related protein- 1 is a negative regulator of trabecular bone formation in adult mice. Mol. Endocrinol., 18, 1222-1237.
37. Popp, M.W. and Maquat, L.E. (2013) Organizing principles of mammalian nonsense-mediated mRNA decay. Annu. Rev. Genet., 47, 139-165.
38. Ishikawa, T., Tamai, Y., Zorn, A.M., Yoshida, H., Seldin, M.F., Nishikawa, S. and Taketo, M.M. (2001) Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development, 128, 25-33.
39. Liu, H., Thurig, S., Mohamed, O., Dufort, D. and Wallace, V.A. (2006) Mapping canonical Wnt signaling in the developing and adult retina. Invest. Ophthalmol. Vis. Sci., 47, 5088-5097.
40. Dorsky, R.I., Sheldahl, L.C. and Moon, R.T. (2002) A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol., 241, 229-237.
41. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B. and Schilling, T.F. (1995) Stages of embryonic development of the zebrafish. Dev. Dyn., 203, 253-310.
42. Gongal, P.A. and Waskiewicz, A.J. (2008) Zebrafish model of holoprosencephaly demonstrates a key role for TGIF in regulating retinoic acid metabolism. Hum. Mol. Genet., 17, 525-538.
43. Olbrich, H., Schmidts, M., Werner, C., Onoufriadis, A., Loges, N.T., Raidt, J., Banki, N.F., Shoemark, A., Burgoyne, T., Al Turki, S. et al. (2012) Recessive HYDIN mutations cause primary ciliary dyskinesia without randomization of left-right body asymmetry. Am. J. Hum. Genet., 91, 672-684.
44. Egeland, T., Pinto, N. and Vigeland, M.D. (2014) A general approach to power calculation for relationship testing. Forensic Sci. Int. Genet., 9, 186-190.