A murine Zic3 transcript with a premature termination codon evades nonsense-mediated decay during axis formation

DMM Disease Models and Mechanisms

Volumn 6, Issue 3, 2013, Pages 755-767

  Ahmed, Jehangir N ^a   Ali, Radiya G ^a   Warr, Nicholas ^b   Wilson, Heather M ^a   Bellchambers, Helen M ^a   Barratt, Kristen S ^a   Thompson, Amelia J ^a   Arkell, Ruth M ^a,b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; COMPLEMENTARY DNA; MUTANT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZIC3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXIS; EMBRYO DEVELOPMENT; GENE MUTATION; IN SITU HYBRIDIZATION; IN VIVO STUDY; MOUSE; MOUSE MUTANT; MUTATIONAL ANALYSIS; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NULL ALLELE; PHENOTYPE; PREMATURE TERMINATION CODON; PRIORITY JOURNAL; STOP CODON; TRANSCRIPTION INITIATION;

ALLELES; ANIMALS; BASE SEQUENCE; BETA CATENIN; CELL NUCLEUS; CODON, NONSENSE; DIFFUSION; EMBRYO, MAMMALIAN; ENDODERM; GASTRULATION; HETEROTAXY SYNDROME; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NONSENSE MEDIATED MRNA DECAY; ORGANOGENESIS; PROTEIN STABILITY; RNA SPLICE SITES; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84877807396     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.011668     Document Type: Article

References (52)

1. Ali, R. G., Bellchambers, H. M. and Arkell, R. M. (2012). Zinc fingers of the cerebellum (Zic): transcription factors and co-factors. Int. J. Biochem. Cell Biol. 44, 2065-2068.
2. Arkell, R. M., Cadman, M., Marsland, T., Southwell, A., Thaung, C., Davies, J. R., Clay, T., Beechey, C. V., Evans, E. P., Strivens, M. A. et al. (2001). Genetic, physical, and phenotypic characterization of the Del(13)Svea36H mouse. Mamm. Genome 12, 687-694.
3. Aruga, J., Nagai, T., Tokuyama, T., Hayashizaki, Y., Okazaki, Y., Chapman, V. M. and Mikoshiba, K. (1996a). The mouse zic gene family. Homologues of the Drosophila pair-rule gene odd-paired. J. Biol. Chem. 271, 1043-1047.
4. Aruga, J., Yozu, A., Hayashizaki, Y., Okazaki, Y., Chapman, V. M. and Mikoshiba, K. (1996b). Identification and characterization of Zic4, a new member of the mouse Zic gene family. Gene 172, 291-294.
5. Aruga, J., Kamiya, A., Takahashi, H., Fujimi, T. J., Shimizu, Y., Ohkawa, K., Yazawa, S., Umesono, Y., Noguchi, H., Shimizu, T. et al. (2006). A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87, 783-792.
6. Bateman, J. F., Freddi, S., Nattrass, G. and Savarirayan, R. (2003). Tissue-specific RNA surveillance? Nonsense-mediated mRNA decay causes collagen X haploinsufficiency in Schmid metaphyseal chondrodysplasia cartilage. Hum. Mol. Genet. 12, 217-225.
7. Bedard, J. E., Purnell, J. D. and Ware, S. M. (2007). Nuclear import and export signals are essential for proper cellular trafficking and function of ZIC3. Hum. Mol. Genet. 16, 187-198.
8. Behrens, J., von Kries, J. P., Kühl, M., Bruhn, L., Wedlich, D., Grosschedl, R. and Birchmeier, W. (1996). Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382, 638-642.
9. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
10. Bogani, D., Warr, N., Elms, P., Davies, J., Tymowska-Lalanne, Z., Goldsworthy, M., Cox, R. D., Keays, D. A., Flint, J., Wilson, V. et al. (2004). New semidominant mutations that affect mouse development. Genesis 40, 109-117.
11. Brown, L., Paraso, M., Arkell, R. and Brown, S. (2005). In vitro analysis of partial loss-of-function ZIC2 mutations in holoprosencephaly: alanine tract expansion modulates DNA binding and transactivation. Hum. Mol. Genet. 14, 411-420.
12. Carrel, T., Purandare, S. M., Harrison, W., Elder, F., Fox, T., Casey, B. and Herman, G. E. (2000). The X-linked mouse mutation Bent tail is associated with a deletion of the Zic3 locus. Hum. Mol. Genet. 9, 1937-1942.
13. Chhin, B., Hatayama, M., Bozon, D., Ogawa, M., Schön, P., Tohmonda, T., Sassolas, F., Aruga, J., Valard, A. G., Chen, S. C. et al. (2007). Elucidation of penetrance variability of a ZIC3 mutation in a family with complex heart defects and functional analysis of ZIC3 mutations in the first zinc finger domain. Hum. Mutat. 28, 563-570.
14. Downs, K. M. and Davies, T. (1993). Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 118, 1255-1266.
15. Elms, P., Siggers, P., Napper, D., Greenfield, A. and Arkell, R. (2003). Zic2 is required for neural crest formation and hindbrain patterning during mouse development. Dev. Biol. 264, 391-406.
16. Elms, P., Scurry, A., Davies, J., Willoughby, C, Hacker, T., Bogani, D. and Arkell, R. (2004). Overlapping and distinct expression domains of Zic2 and Zic3 during mouse gastrulation. Gene Expr. Patterns 4, 505-511.
17. Ferrero, G. B., Gebbia, M., Pilia, G., Witte, D., Peier, A., Hopkin, R. J., Craigen, W. J., Shaffer, L. G., Schlessinger, D., Ballabio, A. et al. (1997). A submicroscopic deletion in Xq26 associated with familial situs ambiguus. Am. J. Hum. Genet. 61, 395-401.
18. Frischmeyer, P. A. and Dietz, H. C. (1999). Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8, 1893-1900.
19. Fujimi, T. J., Hatayama, M. and Aruga, J. (2012). Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/β-catenin signaling pathway. Dev. Biol. 361, 220-231.
20. Furushima, K., Murata, T., Matsuo, I. and Aizawa, S. (2000). A new murine zinc finger gene, Opr. Mech. Dev. 98, 161-164.
21. Garber, E. D. (1952). 'Bent-Tail', a dominant, sex-linked mutation in the mouse. Proc. Natl. Acad. Sci. USA 38, 876-879.
22. Gebbia, M., Ferrero, G. B., Pilia, G., Bassi, M. T., Aylsworth, A., Penman-Splitt, M., Bird, L. M., Bamforth, J. S., Burn, J., Schlessinger, D. et al. (1997). X-linked situs abnormalities result from mutations in ZIC3. Nat. Genet. 17, 305-308.
23. Gudikote, J. P., Imam, J. S., Garcia, R. F. and Wilkinson, M. F. (2005). RNA splicing promotes translation and RNA surveillance. Nat. Struct. Mol. Biol. 12, 801-809.
24. Hatayama, M., Tomizawa, T., Sakai-Kato, K., Bouvagnet, P., Kose, S., Imamoto, N., Yokoyama, S., Utsunomiya-Tate, N., Mikoshiba, K., Kigawa, T. et al. (2008). Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain. Hum. Mol. Genet. 17, 3459-3473.
25. Holbrook, J. A., Neu-Yilik, G., Hentze, M. W. and Kulozik, A. E. (2004). Nonsense-mediated decay approaches the clinic. Nat. Genet. 36, 801-808.
26. Inoue, T., Ota, M., Mikoshiba, K. and Aruga, J. (2007). Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev. Biol. 306, 669-684.
27. Kitaguchi, T., Nagai, T., Nakata, K., Aruga, J. and Mikoshiba, K. (2000). Zic3 is involved in the left-right specification of the Xenopus embryo. Development 127, 4787-4795.
28. Klootwijk, R., Franke, B., van der Zee, C. E., de Boer, R. T., Wilms, W., Hol, F. A. and Mariman, E. C. (2000). A deletion encompassing Zic3 in bent tail, a mouse model for X-linked neural tube defects. Hum. Mol. Genet. 9, 1615-1622.
29. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B. and Clevers, H. (1997). Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/-colon carcinoma. Science 275, 1784-1787.
30. Kovacs, E. M., Ali, R. G., McCormack, A. J. and Yap, A. S. (2002). E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708-6718.
31. Koyabu, Y., Nakata, K., Mizugishi, K., Aruga, J. and Mikoshiba, K. (2001). Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem. 276, 6889-6892.
32. Mahmood, R., Bresnick, J., Hornbruch, A., Mahony, C, Morton, N., Colquhoun, K., Martin, P., Lumsden, A., Dickson, C. and Mason, I. (1995). A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
33. Maquat, L. E. (2004). Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell Biol. 5, 89-99.
34. Mégarbané, A., Salem, N., Stephan, E., Ashoush, R., Lenoir, D., Delague, V., Kassab, R., Loiselet, J. and Bouvagnet, P. (2000). X-linked transposition of the great arteries and incomplete penetrance among males with a nonsense mutation in ZIC3. Eur. J. Hum. Genet. 8, 704-708.
35. Mizugishi, K., Aruga, J., Nakata, K. and Mikoshiba, K. (2001). Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J. Biol. Chem. 276, 2180-2188.
36. Munemitsu, S., Albert, I., Rubinfeld, B. and Polakis, P. (1996). Deletion of an amino-terminal sequence beta-catenin in vivo and promotes hyperphosporylation of the adenomatous polyposis coli tumor suppressor protein. Mol. Cell. Biol. 16, 4088-4094.
37. Nagy, E. and Maquat, L. E. (1998). A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23, 198-199.
38. Neu-Yilik, G., Gehring, N. H., Thermann, R., Frede, U., Hentze, M. W. and Kulozik, A. E. (2001). Splicing and 3' end formation in the definition of nonsense-mediated decay-competent human beta-globin mRNPs. EMBO J. 20, 532-540.
39. Pourebrahim, R., Houtmeyers, R., Ghogomu, S., Janssens, S., Thelie, A., Tran, H. T., Langenberg, T., Vleminckx, K., Bellefroid, E., Cassiman, J. J. et al. (2011). Transcription factor Zic2 inhibits Wnt/β-catenin protein signaling. J. Biol. Chem. 286, 37732-37740.
40. Purandare, S. M., Ware, S. M., Kwan, K. M., Gebbia, M., Bassi, M. T., Deng, J. M., Vogel, H., Behringer, R. R., Belmont, J. W. and Casey, B. (2002). A complex syndrome of left-right axis, central nervous system and axial skeleton defects in Zic3 mutant mice. Development 129, 2293-2302.
41. Rosen, B. and Beddington, R. (1994). Detection of mRNA in whole mounts of mouse embryos using digoxigenin riboprobes. Methods Mol. Biol. 28, 201-208.
42. Salero, E., Pérez-Sen, R., Aruga, J., Giménez, C. and Zafra, F. (2001). Transcription factors Zic1 and Zic2 bind and transactivate the apolipoprotein E gene promoter. J. Biol. Chem. 276, 1881-1888.
43. Sasaki, H. and Hogan, B. L. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
44. Shawlot, W. and Behringer, R. R. (1995). Requirement for Lim1 in head-organizer function. Nature 374, 425-430.
45. Thomsen, N., Ali, R. G., Ahmed, J. N. and Arkell, R. M. (2012). High resolution melt analysis (HRMA); a viable alternative to agarose gel electrophoresis for mouse genotyping. PLoS ONE 7, e45252.
46. Ware, S. M., Peng, J., Zhu, L., Fernbach, S., Colicos, S., Casey, B., Towbin, J. and Belmont, J. W. (2004). Identification and functional analysis of ZIC3 mutations in heterotaxy and related congenital heart defects. Am. J. Hum. Genet. 74, 93-105.
47. Ware, S. M., Harutyunyan, K. G. and Belmont, J. W. (2006a). Heart defects in X-linked heterotaxy: evidence for a genetic interaction of Zic3 with the nodal signaling pathway. Dev. Dyn. 235, 1631-1637.
48. Ware, S. M., Harutyunyan, K. G. and Belmont, J. W. (2006b). Zic3 is critical for early embryonic patterning during gastrulation. Dev. Dyn. 235, 776-785.
49. Wei, X., Henke, V. G., Strübing, C., Brown, E. B. and Clapham, D. E. (2003). Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys. J. 84, 1317-1327.
50. Wilkinson, D. G. (1992). Whole mount in situ hybridisation of vertebrate embryos. In In Situ Hybridisation (ed. D. G. Wilkinson), pp. 75-83. Oxford: IRL Press.
51. Yang, Y., Hwang, C. K., Junn, E., Lee, G. and Mouradian, M. M. (2000). ZIC2 and Sp3 repress Sp1-induced activation of the human D1A dopamine receptor gene. J. Biol. Chem. 275, 38863-38869.
52. Zhu, L., Peng, J. L., Harutyunyan, K. G., Garcia, M. D., Justice, M. J. and Belmont, J. W. (2007). Craniofacial, skeletal, and cardiac defects associated with altered embryonic murine Zic3 expression following targeted insertion of a PGK-NEO cassette. Front. Biosci. 12, 1680-1690.