Apoptotic and proliferative defects characterize ocular development in a microphthalmic BMP model

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 7, 2013, Pages 4636-4647

  French, Curtis R ^a   Stach, Tara R ^a   March, Lindsey D ^a   Lehmann, Ordan J ^a   Waskiewicz, Andrew J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; Bone morphogenetic protein; Forkhead box; Gdf6; Proliferation

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CASPASE 3; FORKHEAD TRANSCRIPTION FACTOR; GROWTH DIFFERENTIATION FACTOR 6;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; COPY NUMBER VARIATION; EMBRYO; EYE DEVELOPMENT; GENE EXPRESSION; GENE MUTATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MICROPHTHALMIA; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; ZEBRA FISH;

APOPTOSIS; BONE MORPHOGENETIC PROTEIN; FORKHEAD BOX; GDF6; PROLIFERATION;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEINS; CELL CYCLE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EMBRYO, NONMAMMALIAN; EYE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 6; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; MICROPHTHALMOS; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84880048636     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11674     Document Type: Article

References (63)

1. Verma AS, Fitzpatrick DR. Anophthalmia and microphthalmia. Orphanet J Rare Dis. 2007;2:47.
2. Morrison D, FitzPatrick D, Hanson I, et al. National study of microphthalmia, anophthalmia, and coloboma (MAC) in Scotland: investigation of genetic aetiology. J Med Genet. 2002;39: 16-22.
3. Parker SE, Mai CT, Canfield MA, et al. Updated National Birth Prevalence estimates for selected birth defects in the United States, 2004-2006. Birth Defects Res Clin Mol Teratol. 2010;88: 1008-1016.
4. Kallen B, Robert E, Harris J. The descriptive epidemiology of anophthalmia and microphthalmia. Int J Epidemiol. 1996;25: 1009-1016.
5. Shaham O, Menuchin Y, Farhy C, Ashery-Padan R. Pax6: a multi-level regulator of ocular development. Prog Ret Eye Res. 2012;31:351-376.
6. Bardakjian TM, Schneider A. The genetics of anophthalmia and microphthalmia. Curr Opin Ophthalmol. 2011;22:309-313.
7. Fuhrmann S. Eye morphogenesis and patterning of the optic vesicle. Curr Top Dev Biol. 2010;93:61-84.
8. Ragge NK, Brown AG, Poloschek CM, et al. Heterozygous mutations of OTX2 cause severe ocular malformations. Amer J Hum Genet. 2005;76:1008-1022.
9. Schilter KF, Schneider A, Bardakjian T, et al. OTX2 microphthalmia syndrome: four novel mutations and delineation of a phenotype. Clin Genet. 2011;79:158-168.
10. Smith AN, Miller LA, Radice G, Ashery-Padan R, Lang RA. Stagedependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development. 2009; 136:2977-2985.
11. Liu W, Lagutin OV, Mende M, Streit A, Oliver G. Six3 activation of Pax6 expression is essential for mammalian lens induction and specification. EMBO J. 2006;25:5383-5395.
12. van Raamsdonk CD, Tilghman SM. Dosage requirement and allelic expression of PAX6 during lens placode formation. Development. 2000;127:5439-5448.
13. Matsushima D, Heavner W, Pevny LH. Combinatorial regulation of optic cup progenitor cell fate by SOX2 and PAX6. Development. 2011;138:443-454.
14. Wen J, Hu Q, Li M, et al. Pax6 directly modulate Sox2 expression in the neural progenitor cells. Neuroreport. 2008; 19:413-417.
15. Martinez-Morales JR, Dolez V, Rodrigo I, et al. OTX2 activates the molecular network underlying retina pigment epithelium differentiation. J Biol Chem. 2003;278:21721-21731.
16. Westenskow P, Piccolo S, Fuhrmann S. Beta-catenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development. 2009;136:2505-2510.
17. Dhomen NS, Balaggan KS, Pearson RA, et al. Absence of chx10 causes neural progenitors to persist in the adult retina. Invest Ophthalmol Vis Sci. 2006;47:386-396.
18. Thiel G. How Sox2 maintains neural stem cell identity. Biochem J. 2013;450:e1-2.
19. Wu LY, Li M, Hinton DR, et al. Microphthalmia resulting from MSX2-induced apoptosis in the optic vesicle. Invest Ophthalmol Vis Sci. 2003;44:2404-2412.
20. Steingrimsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network. Ann Rev Genet. 2004;38:365-411.
21. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol. 2006;6:36.
22. Nuckels RJ, Ng A, Darland T, Gross JM. The vacuolar-ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Invest Ophthalmol Vis Sci. 2009;50:893-905.
23. Bakrania P, Efthymiou M, Klein JC, et al. Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways. Amer J Hum Genet. 2008;82:304-319.
24. Reis LM, Tyler RC, Schilter KF, et al. BMP4 loss-of-function mutations in developmental eye disorders including SHORT syndrome. Hum Genet. 2011;130:495-504.
25. Ye M, Berry-Wynne KM, Asai-Coakwell M, et al. Mutation of the bone morphogenetic protein GDF3 causes ocular and skeletal anomalies. Hum Mol Genet. 2010;19:287-298.
26. Trousse F, Esteve P, Bovolenta P. Bmp4 mediates apoptotic cell death in the developing chick eye. J Neurosci. 2001;21:1292-1301.
27. Asai-Coakwell M, French CR, Berry KM, et al. GDF6, a novel locus for a spectrum of ocular developmental anomalies. Amer J Hum Genet. 2007;80:306-315.
28. Asai-Coakwell M, French CR, Ye M, et al. Incomplete penetrance and phenotypic variability characterize Gdf6-attributable oculo-skeletal phenotypes. Hum Mol Genet. 2009;18:1110-1121.
29. Gonzalez-Rodriguez J, Pelcastre EL, Tovilla-Canales JL, et al. Mutational screening of CHX10, GDF6, OTX2, RAX and SOX2 genes in 50 unrelated microphthalmia-anophthalmia-coloboma (MAC) spectrum cases. Brit J Ophthalmol. 2010;94:1100-1104.
30. Huillard E, Laugier D, Marx M. Defects in chicken neuroretina misexpressing the BMP antagonist Drm/Gremlin. Dev Biol. 2005;283:335-344.
31. Webb TR, Matarin M, Gardner JC, et al. X-linked megalocornea caused by mutations in CHRDL1 identifies an essential role for ventroptin in anterior segment development. Amer J Hum Genet. 2012;90:247-259.
32. Paulsen M, Legewie S, Eils R, Karaulanov E, Niehrs C. Negative feedback in the bone morphogenetic protein 4 (BMP4) synexpression group governs its dynamic signaling range and canalizes development. Proc Natl Acad Sci U S A. 2011;108: 10202-10207.
33. French CR, Erickson T, French DV, Pilgrim DB, Waskiewicz AJ. Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development. Dev Biol. 2009;333:37-47.
34. Gosse NJ, Baier H. An essential role for Radar (Gdf6a) in inducing dorsal fate in the zebrafish retina. Proc Natl Acad Sci U S A. 2009;106:2236-2241.
35. Hanel ML, Hensey C. Eye and neural defects associated with loss of GDF6. BMC Dev Biol. 2006;6:43.
36. den Hollander AI, Biyanwila J, Kovach P, et al. Genetic defects of GDF6 in the zebrafish out of sight mutant and in human eye developmental anomalies. BMC Genet. 2010;11:102.
37. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet. 2009; 10:233-240.
38. Myatt SS, Lam EW. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer. 2007;7:847-859.
39. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253-310.
40. Gongal PA, Waskiewicz AJ. Zebrafish model of holoprosencephaly demonstrates a key role for TGIF in regulating retinoic acid metabolism. Hum Mol Genet. 2008;17:525-538.
41. Thisse C, Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc. 2008;3:59-69.
42. Pieper AA, Xie S, Capota E, et al. Discovery of a proneurogenic, neuroprotective chemical. Cell. 2010;142:39-51.
43. Berry FB, Lines MA, Oas JM, et al. Functional interactions between FOXC1 and PITX2 underlie the sensitivity to FOXC1 gene dose in Axenfeld-Rieger syndrome and anterior segment dysgenesis. Hum Mol Genet. 2006;15:905-919.
44. Seo S, Singh HP, Lacal PM, et al. Forkhead box transcription factor FoxC1 preserves corneal transparency by regulating vascular growth. Proc Natl Acad Sci U S A. 2012;109:2015-2020.
45. Semina EV, Brownell I, Mintz-Hittner HA, Murray JC, Jamrich M. Mutations in the human forkhead transcription factor FOXE3 associated with anterior segment ocular dysgenesis and cataracts. Hum Mol Genet. 2001;10:231-236.
46. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron. 1995;14:1141-1152.
47. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A. 1996;93:589-595.
48. Wehman AM, Staub W, Meyers JR, Raymond PA, Baier H. Genetic dissection of the zebrafish retinal stem-cell compartment. Dev Biol. 2005;281:53-65.
49. Bielen H, Houart C. BMP signaling protects telencephalic fate by repressing eye identity and its Cxcr4-dependent morphogenesis. Dev Cell. 2012;23:812-822.
50. Asai-Coakwell M, March L, Dai XH, et al. Contribution of growth differentiation factor 6-dependent cell survival to earlyonset retinal dystrophies. Hum Mol Genet. 2013;22:1432-1442.
51. Dang CV. MYC on the path to cancer. Cell. 2012;149:22-35.
52. Bessa J, Tavares MJ, Santos J, et al. meis1 regulates cyclin D1 and c-myc expression, and controls the proliferation of the multipotent cells in the early developing zebrafish eye. Development. 2008;135:799-803.
53. Boisset G, Schorderet DF. Zebrafish hmx1 promotes retinogenesis. Exp Eye Res. 2012;105:34-42.
54. Willer GB, Lee VM, Gregg RG, Link BA. Analysis of the Zebrafish perplexed mutation reveals tissue-specific roles for de novo pyrimidine synthesis during development. Genetics. 2005;170:1827-1837.
55. Murali D, Yoshikawa S, Corrigan RR, et al. Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development. 2005;132: 913-923.
56. Solomon KS, Kudoh T, Dawid IB, Fritz A. Zebrafish foxi1 mediates otic placode formation and jaw development. Development. 2003;130:929-940.
57. Nissen RM, Yan J, Amsterdam A, Hopkins N, Burgess SM. Zebrafish foxi one modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning. Development. 2003;130:2543-2554.
58. Hulander M, Wurst W, Carlsson P, Enerback S. The winged helix transcription factor Fkh10 is required for normal development of the inner ear. Nat Genet. 1998;20:374-376.
59. Solomon KS, Logsdon JM Jr, Fritz A. Expression and phylogenetic analyses of three zebrafish FoxI class genes. Dev Dyn. 2003;228:301-307.
60. Ohyama T, Groves AK. Expression of mouse Foxi class genes in early craniofacial development. Dev Dyn. 2004;231:640-646.
61. Wijchers PJ, Hoekman MF, Burbach JP, Smidt MP. Cloning and analysis of the murine Foxi2 transcription factor. Biochim Biophys Acta. 2005;1731:133-138.
62. Cha SW, McAdams M, Kormish J, Wylie C, Kofron M. Foxi2 is an animally localized maternal mRNA in Xenopus, and an activator of the zygotic ectoderm activator Foxi1e. PLoS One. 2012;7:e41782.
63. Amsterdam A, Burgess S, Golling G, et al. A large-scale insertional mutagenesis screen in zebrafish. Genes Dev. 1999;13:2713-2724.