Zic3 is required in the migrating primitive streak for node morphogenesis and left-right patterning

Human Molecular Genetics

Volumn 22, Issue 10, 2013, Pages 1913-1923

  Sutherland, Mardi J ^a   Wang, Shuyun ^b   Quinn, Malgorzata E ^a   Haaning, Allison ^a   Ware, Stephanie M ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CRE RECOMBINASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN OF THE CEREBELLUM 3;

ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ECTODERM; EMBRYO; FEMALE; GASTRULATION; GENE DELETION; GENOTYPE; HEART; HEART DEVELOPMENT; HEART LEFT RIGHT SHUNT; MALE; MESODERM; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE SPECIFICITY;

ANIMALS; DEXTROCARDIA; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC DISEASES, X-LINKED; HEART; HETEROTAXY SYNDROME; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, MUTANT STRAINS; ORGANOGENESIS; TRANSCRIPTION FACTORS;

MUS;

EID: 84877021428     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt001     Document Type: Article

References (59)

1. Gelb, B.D. (2004) Genetic basis of congenital heart disease. Curr. Opin. Cardiol., 19, 110-115.
2. Hoffman, J.I. (1995) Incidence of congenital heart disease: II. Prenatal incidence. Pediatr. Cardiol., 16, 155-165.
3. Sutherland, M.J. and Ware, S.M. (2009) Disorders of left-right asymmetry: heterotaxy and situs inversus. Am. J. Med. Genet. C. Semin. Med. Genet., 151C, 307-317.
4. 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.
5. 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.
6. Megarbane, 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.
7. 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.
8. Ware, S.M., Harutyunyan, K.G. and Belmont, J.W. (2006) Zic3 is critical for early embryonic patterning during gastrulation. Dev. Dyn., 235, 776-785.
9. Ware, S.M., Harutyunyan, K.G. and Belmont, J.W. (2006) Heart defects in X-linked heterotaxy: evidence for a genetic interaction of Zic3 with the nodal signaling pathway. Dev. Dyn., 235, 1631-1637.
10. Cast, A.E., Gao, C., Amack, J.D. and Ware, S.M. (2012) An essential and highly conserved role for Zic3 in left-right patterning, gastrulation and convergent extension morphogenesis. Dev. Biol., 364, 22-31.
11. Kinder, S.J., Tsang, T.E., Quinlan, G.A., Hadjantonakis, A.K., Nagy, A. and Tam, P.P. (1999) The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development, 126, 4691-4701.
12. Kinder, S.J., Tsang, T.E., Wakamiya, M., Sasaki, H., Behringer, R.R., Nagy, A. and Tam, P.P. (2001) The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. Development, 128, 3623-3634.
13. Robb, L. and Tam, P.P. (2004) Gastrula organiser and embryonic patterning in the mouse. Semin. Cell Dev. Biol., 15, 543-554.
14. Beddington, R.S. (1994) Induction of a second neural axis by the mouse node. Development, 120, 613-620.
15. Lee, J.D. and Anderson, K.V. (2008) Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn., 237, 3464-3476.
16. Collignon, J., Varlet, I. and Robertson, E.J. (1996) Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature, 381, 155-158.
17. Lowe, L.A., Supp, D.M., Sampath, K., Yokoyama, T., Wright, C.V., Potter, S.S., Overbeek, P. and Kuehn, M.R. (1996) Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature, 381, 158-161.
18. Brennan, J., Norris, D.P. and Robertson, E.J. (2002) Nodal activity in the node governs left-right asymmetry. Genes. Dev., 16, 2339-2344.
19. Saijoh, Y., Oki, S., Ohishi, S. and Hamada, H. (2003) Left-right patterning of the mouse lateral plate requires nodal produced in the node. Dev. Biol., 256, 160-172.
20. Meno, C., Ito, Y., Saijoh, Y., Matsuda, Y., Tashiro, K., Kuhara, S. and Hamada, H. (1997) Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos. Genes Cells, 2, 513-524.
21. Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y. and Hamada, H. (1996) Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos. Nature, 381, 151-155.
22. Yoshioka, H., Meno, C., Koshiba, K., Sugihara, M., Itoh, H., Ishimaru, Y., Inoue, T., Ohuchi, H., Semina, E.V., Murray, J.C. et al. (1998) Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell, 94, 299-305.
23. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002) Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet., 3, 103-113.
24. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell, 95, 829-837.
25. Okada, Y., Nonaka, S., Tanaka, Y., Saijoh, Y., Hamada, H. and Hirokawa, N. (1999) Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell, 4, 459-468.
26. Brand, T. (2003) Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol., 258, 1-19.
27. Manner, J. (2009) The anatomy of cardiac looping: a step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin. Anat., 22, 21-35.
28. Zhu, L., Harutyunyan, K.G., Peng, J.L., Wang, J., Schwartz, R.J. and Belmont, J.W. (2007) Identification of a novel role of ZIC3 in regulating cardiac development. Hum. Mol. Genet., 16, 1649-1660.
29. Quinn, M.E., Haaning, A. and Ware, S.M. (2012) Preaxial polydactyly caused by Gli3 haploinsufficiency is rescued by Zic3 loss of function in mice. Hum. Mol. Genet., 21, 1888-1896.
30. Moses, K.A., DeMayo, F., Braun, R.M., Reecy, J.L. and Schwartz, R.J. (2001) Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis, 31, 176-180.
31. Verzi, M.P., McCulley, D.J., De Val, S., Dodou, E. and Black, B.L. (2005) The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol., 287, 134-145.
32. Danielian, P.S., Muccino, D., Rowitch, D.H., Michael, S.K. and McMahon, A.P. (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol., 8, 1323-1326.
33. Parsons, S.A., Millay, D.P., Wilkins, B.J., Bueno, O.F., Tsika, G.L., Neilson, J.R., Liberatore, C.M., Yutzey, K.E., Crabtree, G.R., Tsika, R.W. et al. (2004) Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. J. Biol. Chem., 279, 26192-26200.
34. 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.
35. Kumar, A., Lualdi, M., Lewandoski, M. and Kuehn, M.R. (2008) Broad mesodermal and endodermal deletion of Nodal at postgastrulation stages results solely in left/right axial defects. Dev. Dyn., 237, 3591-3601.
36. Perantoni, A.O., Timofeeva, O., Naillat, F., Richman, C., Pajni-Underwood, S., Wilson, C., Vainio, S., Dove, L.F. and Lewandoski, M. (2005) Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development, 132, 3859-3871.
37. Clements, D., Taylor, H.C., Herrmann, B.G. and Stott, D. (1996) Distinct regulatory control of the Brachyury gene in axial and non-axial mesoderm suggests separation of mesoderm lineages early in mouse gastrulation. Mech. Dev., 56, 139-149.
38. Zhang, Y., Huang, G., Shornick, L.P., Roswit, W.T., Shipley, J.M., Brody, S.L. and Holtzman, M.J. (2007) A transgenic FOXJ1-Cre system for gene inactivation in ciliated epithelial cells. Am. J. Respir. Cell Mol. Biol., 36, 515-519.
39. Wang, S. and Ware, S.M. (2009) Use of FOXJ1CreER2T mice for inducible deletion of embryonic node gene expression. Genesis, 47, 132-136.
40. Blatt, E.N., Yan, X.H., Wuerffel, M.K., Hamilos, D.L. and Brody, S.L. (1999) Forkhead transcription factor HFH-4 expression is temporally related to ciliogenesis. Am. J. Respir. Cell Mol. Biol., 21, 168-176.
41. Brody, S.L., Yan, X.H., Wuerffel, M.K., Song, S.K. and Shapiro, S.D. (2000) Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol., 23, 45-51.
42. Sulik, K., Dehart, D.B., Iangaki, T., Carson, J.L., Vrablic, T., Gesteland, K. and Schoenwolf, G.C. (1994) Morphogenesis of the murine node and notochordal plate. Dev. Dyn., 201, 260-278.
43. Yamanaka, Y., Tamplin, O.J., Beckers, A., Gossler, A. and Rossant, J. (2007) Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms. Dev. Cell, 13, 884-896.
44. Lee, J.D., Migeotte, I. and Anderson, K.V. (2010) Left-right patterning in the mouse requires Epb4.1l5-dependent morphogenesis of the node and midline. Dev. Biol., 346, 237-246.
45. Migeotte, I., Grego-Bessa, J. and Anderson, K.V. (2011) Rac1 mediates morphogenetic responses to intercellular signals in the gastrulating mouse embryo. Development, 138, 3011-3020.
46. Pulina, M.V., Hou, S.Y., Mittal, A., Julich, D., Whittaker, C.A., Holley, S.A., Hynes, R.O. and Astrof, S. (2011) Essential roles of fibronectin in the development of the left-right embryonic body plan. Dev. Biol., 354, 208-220.
47. Krebs, L.T., Iwai, N., Nonaka, S., Welsh, I.C., Lan, Y., Jiang, R., Saijoh, Y., O'Brien, T.P., Hamada, H. and Gridley, T. (2003) Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes. Dev., 17, 1207-1212.
48. Przemeck, G.K., Heinzmann, U., Beckers, J. and Hrabe de Angelis, M. (2003) Node and midline defects are associated with left-right development in Delta1 mutant embryos. Development, 130, 3-13.
49. Takeuchi, J.K., Lickert, H., Bisgrove, B.W., Sun, X., Yamamoto, M., Chawengsaksophak, K., Hamada, H., Yost, H.J., Rossant, J. and Bruneau, B.G. (2007) Baf60c is a nuclear Notch signaling component required for the establishment of left-right asymmetry. Proc. Natl Acad. Sci. USA, 104, 846-851.
50. Merrill, B.J., Pasolli, H.A., Polak, L., Rendl, M., Garcia-Garcia, M.J., Anderson, K.V. and Fuchs, E. (2004) Tcf3: a transcriptional regulator of axis induction in the early embryo. Development, 131, 263-274.
51. Fujiwara, T., Dehart, D.B., Sulik, K.K. and Hogan, B.L. (2002) Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse. Development, 129, 4685-4696.
52. Hirokawa, N., Tanaka, Y. and Okada, Y. (2012) Cilia, KIF3 molecular motor and nodal flow. Curr. Opin. Cell Biol., 24, 31-39.
53. Bisgrove, B.W. and Yost, H.J. (2006) The roles of cilia in developmental disorders and disease. Development, 133, 4131-4143.
54. Beckers, A., Alten, L., Viebahn, C., Andre, P. and Gossler, A. (2007) The mouse homeobox gene Noto regulates node morphogenesis, notochordal ciliogenesis, and left-right patterning. Proc. Natl Acad. Sci. USA, 104, 15765-15770.
55. Alten, L., Schuster-Gossler, K., Beckers, A., Groos, S., Ulmer, B., Hegermann, J., Ochs, M. and Gossler, A. (2012) Differential regulation of node formation, nodal ciliogenesis and cilia positioning by Noto and Foxj1. Development, 139, 1276-1284.
56. Antic, D., Stubbs, J.L., Suyama, K., Kintner, C., Scott, M.P. and Axelrod, J.D. (2010) Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One, 5, e8999.
57. Song, H., Hu, J., Chen, W., Elliott, G., Andre, P., Gao, B. and Yang, Y. (2010) Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature, 466, 378-382.
58. Hayashi, S., Lewis, P., Pevny, L. and McMahon, A.P. (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Gene Expr. Patterns, 2, 93-97.
59. Ostrowski, L.E., Hutchins, J.R., Zakel, K. and O'Neal, W.K. (2003) Targeting expression of a transgene to the airway surface epithelium using a ciliated cell-specific promoter. Mol. Ther., 8, 637-645.