Loss of Cited2 causes congenital heart disease by perturbing left-right patterning of the body axis

Human Molecular Genetics

Volumn 20, Issue 6, 2011, Pages 1097-1110

  Floro, Kylie Lopes ^a   Artap, Stanley T ^a   Preis, Jost I ^a   Fatkin, Diane ^a,b,c   Chapman, Gavin ^a,b   Furtado, Milena B ^a,e   Harvey, Richard P ^a,b   Hamada, Hiroshi ^d   Sparrow, Duncan B ^a,b   Dunwoodie, Sally L ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

^d OSAKA UNIVERSITY   (Japan)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; PROTEIN CITED2; PROTEIN NODAL; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGENITAL HEART DISEASE; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONAL TISSUE; GENE DELETION; GENE LOSS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPE; HEART DEVELOPMENT; HETEROZYGOSITY; IN SITU HYBRIDIZATION; LATERAL PLATE MESODERM; MALE; MAMMAL; MESODERM; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; TRANSTHORACIC ECHOCARDIOGRAPHY;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; HEART; HEART DEFECTS, CONGENITAL; HUMANS; MALE; MESODERM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

MAMMALIA; MUS;

EID: 79952012639     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq554     Document Type: Article

References (90)

1. Aylsworth, A.S. (2001) Clinical aspects of defects in the determination of laterality. Am. J. Med. Genet., 101, 345-355.
2. Lin, A.E., Ticho, B.S., Houde, K., Westgate, M.N. and Holmes, L.B. (2000) Heterotaxy: associated conditions and hospital-based prevalence in newborns. Genet. Med., 2, 157-172.
3. Hoffman, J.I. and Kaplan, S. (2002) The incidence of congenital heart disease. J. Am. Coll. Cardiol., 39, 1890-1900.
4. Dunwoodie, S.L., Rodriguez, T.A. and Beddington, R.S. (1998) Msg1 and Mrg1, founding members of a gene family, show distinct patterns of gene expression during mouse embryogenesis. Mech. Dev., 72, 27-40.
5. Shioda, T., Fenner, M.H. and Isselbacher, K.J. (1997) MSG1 and its related protein MRG1 share a transcription activating domain. Gene, 204, 235-241.
6. Sun, H.B., Zhu, Y.X., Yin, T., Sledge, G. and Yang, Y.C. (1998) MRG1, the product of a melanocyte-specific gene related gene, is a cytokine-inducible transcription factor with transformation activity. Proc. Natl Acad. Sci. USA, 95, 13555-13560.
7. Bhattacharya, S., Michels, C.L., Leung, M.K., Arany, Z.P., Kung, A.L. and Livingston, D.M. (1999) Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev., 13, 64-75.
8. Chou, Y.T., Wang, H., Chen, Y., Danielpour, D. and Yang, Y.C. (2006) Cited2 modulates TGF-beta-mediated upregulation of MMP9. Oncogene, 25, 5547-5560.
9. Bamforth, S.D., Braganca, J., Eloranta, J.J., Murdoch, J.N., Marques, F.I., Kranc, K.R., Farza, H., Henderson, D.J., Hurst, H.C. and Bhattacharya, S. (2001) Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat. Genet., 29, 469-474.
10. Bamforth, S.D., Braganca, J., Farthing, C.R., Schneider, J.E., Broadbent, C., Michell, A.C., Clarke, K., Neubauer, S., Norris, D., Brown, N.A. et al. (2004) Cited2 controls left-right patterning and heart development through a Nodal-Pitx2c pathway. Nat. Genet., 36, 1189-1196.
11. Glenn, D.J. and Maurer, R.A. (1999) MRG1 binds to the LIM domain of Lhx2 and may function as a coactivator to stimulate glycoprotein hormone alpha-subunit gene expression. J. Biol. Chem., 274, 36159-36167.
12. Tien, E.S., Davis, J.W. and Vanden Heuvel, J.P. (2004) Identification of the CREB-binding protein/p300-interacting protein CITED2 as a peroxisome proliferator-activated receptor alpha coregulator. J. Biol. Chem., 279, 24053-24063.
13. Yahata, T., Shao, W., Endoh, H., Hur, J., Coser, K.R., Sun, H., Ueda, Y., Kato, S., Isselbacher, K.J., Brown, M. et al. (2001) Selective coactivation of estrogen-dependent transcription by CITED1 CBP/p300-binding protein. Genes Dev., 15, 2598-2612.
14. Val, P., Martinez-Barbera, J.P. and Swain, A. (2007) Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development, 134, 2349-2358.
15. Qu, X., Lam, E., Doughman, Y.Q., Chen, Y., Chou, Y.T., Lam, M., Turakhia, M., Dunwoodie, S.L., Watanabe, M., Xu, B. et al. (2007) Cited2, a coactivator of HNF4alpha, is essential for liver development. EMBO J., 26, 4445-4456.
16. Weninger, W.J., Lopes Floro, K., Bennett, M.B., Withington, S.L., Preis, J.I., Barbera, J.P., Mohun, T.J. and Dunwoodie, S.L. (2005) Cited2 is required both for heart morphogenesis and establishment of the left-right axis in mouse development. Development, 132, 1337-1348.
17. Barbera, J.P., Rodriguez, T.A., Greene, N.D., Weninger, W.J., Simeone, A., Copp, A.J., Beddington, R.S. and Dunwoodie, S. (2002) Folic acid prevents exencephaly in Cited2 deficient mice. Hum. Mol. Genet., 11, 283-293.
18. Yin, Z., Haynie, J., Yang, X., Han, B., Kiatchoosakun, S., Restivo, J., Yuan, S., Prabhakar, N.R., Herrup, K., Conlon, R.A. et al. (2002) The essential role of Cited2, a negative regulator for HIF-1alpha, in heart development and neurulation. Proc. Natl Acad. Sci., 99, 10488-10493.
19. Withington, S.L., Scott, A.N., Saunders, D.N., Lopes Floro, K., Preis, J.I., Michalicek, J., Maclean, K., Sparrow, D.B., Barbera, J.P. and Dunwoodie, S.L. (2006) Loss of Cited2 affects trophoblast formation and vascularization of the mouse placenta. Dev. Biol., 294, 67-82.
20. Chen, Y., Haviernik, P., Bunting, K.D. and Yang, Y.C. (2007) Cited2 is required for normal hematopoiesis in the murine fetal liver. Blood, 110, 2889-2898.
21. Xu, B., Qu, X., Gu, S., Doughman, Y.Q., Watanabe, M., Dunwoodie, S.L. and Yang, Y.C. (2008) Cited2 is required for fetal lung maturation. Dev. Biol., 317, 95-105.
22. Chen, Y., Doughman, Y.Q., Gu, S., Jarrell, A., Aota, S., Cvekl, A., Watanabe, M., Dunwoodie, S.L., Johnson, R.S., van Heyningen, V. et al. (2008) Cited2 is required for the proper formation of the hyaloid vasculature and for lens morphogenesis. Development, 135, 2939-2948.
23. Chen, Y., Carlson, E.C., Chen, Z.Y., Hamik, A., Jain, M.K., Dunwoodie, S.L. and Yang, Y.C. (2009) Conditional deletion of Cited2 results in defective corneal epithelial morphogenesis and maintenance. Dev. Biol., 334, 243-252.
24. Buaas, F.W., Val, P. and Swain, A. (2009) The transcription co-factor CITED2 functions during sex determination and early gonad development. Hum. Mol. Genet., 18, 2989-3001.
25. Combes, A.N., Spiller, C.M., Harley, V.R., Sinclair, A.H., Dunwoodie, S.L., Wilhelm, D. and Koopman, P. (2009) Gonadal defects in Cited2-mutant mice indicate a role for SF1 in both testis and ovary differentiation. Int. J. Dev. Biol., 54, 683-689.
26. Sperling, S., Grimm, C.H., Dunkel, I., Mebus, S., Sperling, H.P., Ebner, A., Galli, R., Lehrach, H., Fusch, C., Berger, F. et al. (2005) Identification and functional analysis of CITED2 mutations in patients with congenital heart defects. Hum. Mutat., 26, 575-582.
27. Yang, X.F., Wu, X.Y., Li, M., Li, Y.G., Dai, J.T., Bai, Y.H. and Tian, J. (2010) [Mutation analysis of Cited2 in patients with congenital heart disease. Zhonghua Er Ke Za Zhi, 48, 293-296.
28. MacDonald, S.T., Bamforth, S.D., Chen, C.M., Farthing, C.R., Franklyn, A., Broadbent, C., Schneider, J.E., Saga, Y., Lewandoski, M. and Bhattacharya, S. (2008) Epiblastic Cited2 deficiency results in cardiac phenotypic heterogeneity and provides a mechanism for haploinsufficiency. Cardiovasc. Res., 79, 448-457.
29. Maclean, K. and Dunwoodie, S.L. (2004) Breaking symmetry: a clinical overview of left-right patterning. Clin. Genet., 65, 441-457.
30. Hutchins, G.M., Moore, G.W., Lipford, E.H., Haupt, H.M. and Walker, M.C. (1983) Asplenia and polysplenia malformation complexes explained by abnormal embryonic body curvature. Pathol. Res. Pract., 177, 60-76.
31. Rose, V., Izukawa, T. and Moes, C.A. (1975) Syndromes of asplenia and polysplenia. A review of cardiac and non-cardiac malformations in 60 cases withspecial reference to diagnosis and prognosis. Br. Heart J., 37, 840-852.
32. Ruttenberg, H.D., Neufeld, H.N., Lucas, R.V. Jr, Carey, L.S., Adams, P. Jr, Anderson, R.C. and Edwards, J.E. (1964) Syndrome of congenital cardiac disease with asplenia. Distinction from other forms of congenital cyanotic cardiac disease. Am. J. Cardiol., 13, 387-406.
33. Van Mierop, L. and Wiglesworth, F. (1962) Isomerism of the cardiac atria in the asplenia syndrome. Lab. Invest., 11, 1303-1315.
34. Arnold, G.L., Bixler, D. and Girod, D. (1983) Probable autosomal recessive inheritance of polysplenia, situs inversus and cardiac defects in an Amish family. Am. J. Med. Genet., 16, 35-42.
35. Katcher, A.L. (1980) Familial asplenia, other malformations, and sudden death. Pediatrics, 65, 633-635.
36. Zlotogora, J., Schimmel, M.S. and Glaser, Y. (1987) Familial situs inversus and congenital heart defects. Am. J. Med. Genet., 26, 181-184.
37. Burn, J. (1991) Disturbance of morphological laterality in humans. Ciba Found. Symp., 162, 282-296; discussion 296-289.
38. Bamford, R.N., Roessler, E., Burdine, R.D., Saplakoglu, U., dela Cruz, J., Splitt, M., Goodship, J.A., Towbin, J., Bowers, P., Ferrero, G.B. et al. (2000) Loss-of-function mutations in the EGF-CFC gene CFC1 are associated with human left-right laterality defects. Nat. Genet., 26, 365-369.
39. Goldmuntz, E., Bamford, R., Karkera, J.D., dela Cruz, J., Roessler, E. and Muenke, M. (2002) CFC1 mutations in patients with transposition of the great arteries and double-outlet right ventricle. Am. J. Hum. Genet., 70, 776-780.
40. Roessler, E., Pei, W., Ouspenskaia, M.V., Karkera, J.D., Velez, J.I., Banerjee-Basu, S., Gibney, G., Lupo, P.J., Mitchell, L.E., Towbin, J.A. et al. (2009) Cumulative ligand activity of NODAL mutations and modifiers are linked to human heart defects and holoprosencephaly. Mol. Genet. Metab., 98, 225-234.
41. Constam, D.B. and Robertson, E.J. (2000) SPC4/PACE4 regulates a TGFbeta signaling network during axis formation. Genes Dev., 14, 1146-1155.
42. Marques, S., Borges, A.C., Silva, A.C., Freitas, S., Cordenonsi, M. and Belo, J.A. (2004) The activity of the Nodal antagonist Cerl-2 in the mouse node is required for correct L/R body axis. Genes Dev., 18, 2342-2347.
43. Meno, C., Shimono, A., Saijoh, Y., Yashiro, K., Mochida, K., Ohishi, S., Noji, S., Kondoh, H. and Hamada, H. (1998) lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell, 94, 287-297.
44. Weninger, W.J. and Mohun, T. (2002) Phenotyping transgenic embryos: a rapid 3-D screening method based on episcopic fluorescence image capturing. Nat. Genet., 30, 59-65.
45. Christoffels, V.M., Mommersteeg, M.T., Trowe, M.O., Prall, O.W., de Gier-de Vries, C., Soufan, A.T., Bussen, M., Schuster-Gossler, K., Harvey, R.P., Moorman, A.F. et al. (2006) Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ. Res., 98, 1555-1563.
46. Prall, O.W., Menon, M.K., Solloway, M.J., Watanabe, Y., Zaffran, S., Bajolle, F., Biben, C., McBride, J.J., Robertson, B.R., Chaulet, H. et al. (2007) An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell, 128, 947-959.
47. Stanley, E.G., Biben, C., Elefanty, A., Barnett, L., Koentgen, F., Robb, L. and Harvey, R.P. (2002) Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3'UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int. J. Dev. Biol., 46, 431-439.
48. Preis, J.I., Wise, N., Solloway, M.J., Harvey, R.P., Sparrow, D.B. and Dunwoodie, S.L. (2006) Generation of conditional Cited2 null alleles. Genesis, 44, 579-583.
49. Xu, B., Doughman, Y., Turakhia, M., Jiang, W., Landsettle, C.E., Agani, F.H., Semenza, G.L., Watanabe, M. and Yang, Y.C. (2007) Partial rescue of defects in Cited2-deficient embryos by HIF-1alpha heterozygosity. Dev. Biol., 301, 130-140.
50. Collignon, J., Varlet, I. and Robertson, E.J. (1996) Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature, 381, 155-158.
51. 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.
52. Zhou, X., Sasaki, H., Lowe, L., Hogan, B.L. and Kuehn, M.R. (1993) Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature, 361, 543-547.
53. Pearce, J.J., Penny, G. and Rossant, J. (1999) A mouse cerberus/Dan-related gene family. Dev. Biol., 209, 98-110.
54. 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.
55. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. and Inoue, T. (1999) MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development, 126, 3437-3447.
56. Yamamoto, M., Mine, N., Mochida, K., Sakai, Y., Saijoh, Y., Meno, C. and Hamada, H. (2003) Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development, 130, 1795-1804.
57. Saijoh, Y., Adachi, H., Sakuma, R., Yeo, C.Y., Yashiro, K., Watanabe, M., Hashiguchi, H., Mochida, K., Ohishi, S., Kawabata, M. et al. (2000) Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Mol. Cell, 5, 35-47.
58. Shiratori, H., Sakuma, R., Watanabe, M., Hashiguchi, H., Mochida, K., Sakai, Y., Nishino, J., Saijoh, Y., Whitman, M. and Hamada, H. (2001) Two-step regulation of left-right asymmetric expression of Pitx2: initiation by nodal signaling and maintenance by Nkx2. Mol. Cell, 7, 137-149.
59. Shiratori, H. and Hamada, H. (2006) The left-right axis in the mouse: from origin to morphology. Development, 133, 2095-2104.
60. Adachi, H., Saijoh, Y., Mochida, K., Ohishi, S., Hashiguchi, H., Hirao, A. and Hamada, H. (1999) Determination of left/right asymmetric expression of nodal by a left side-specific enhancer with sequence similarity to a lefty-2 enhancer. Genes Dev., 13, 1589-1600.
61. Norris, D.P., Brennan, J., Bikoff, E.K. and Robertson, E.J. (2002) The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development, 129, 3455-3468.
62. Norris, D.P. and Robertson, E.J. (1999) Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements. Genes Dev., 13, 1575-1588.
63. Saijoh, Y., Oki, S., Tanaka, C., Nakamura, T., Adachi, H., Yan, Y.T., Shen, M.M. and Hamada, H. (2005) Two nodal-responsive enhancers control left-right asymmetric expression of Nodal. Dev. Dyn., 232, 1031-1036.
64. Vincent, S.D., Norris, D.P., Le Good, J.A., Constam, D.B. and Robertson, E.J. (2004) Asymmetric Nodal expression in the mouse is governed by the combinatorial activities of two distinct regulatory elements. Mech. Dev., 121, 1403-1415.
65. Braganca, J., Eloranta, J.J., Bamforth, S.D., Ibbitt, J.C., Hurst, H.C. and Bhattacharya, S. (2003) Physical and functional interactions among AP-2 transcription factors, p300/CREB-binding protein, and CITED2. J. Biol. Chem., 278, 16021-16029.
66. Chou, Y.T. and Yang, Y.C. (2006) Post-transcriptional control of Cited2 by transforming growth factor beta: regulation via Smads and Cited2 coding region. J. Biol. Chem., 281, 18451-18462.
67. Yokota, H., Goldring, M.B. and Sun, H.B. (2003) CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J. Biol. Chem., 278, 47275-47280.
68. Nakao, A., Imamura, T., Souchelnytskyi, S., Kawabata, M., Ishisaki, A., Oeda, E., Tamaki, K., Hanai, J., Heldin, C.H., Miyazono, K. et al. (1997) TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J., 16, 5353-5362.
69. Brennan, J., Norris, D.P. and Robertson, E.J. (2002) Nodal activity in the node governs left-right asymmetry. Genes Dev., 16, 2339-2344.
70. Furtado, M.B., Solloway, M.J., Jones, V.J., Costa, M.W., Biben, C., Wolstein, O., Preis, J.I., Sparrow, D.B., Saga, Y., Dunwoodie, S.L. et al. (2008) BMP/SMAD1 signaling sets a threshold for the left/right pathway in lateral plate mesoderm and limits availability of SMAD4. Genes Dev., 22, 3037-3049.
71. 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.
72. Nakamura, T., Mine, N., Nakaguchi, E., Mochizuki, A., Yamamoto, M., Yashiro, K., Meno, C. and Hamada, H. (2006) Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev. Cell, 11, 495-504.
73. 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.
74. 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.
75. Rankin, C.T., Bunton, T., Lawler, A.M. and Lee, S.J. (2000) Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat. Genet., 24, 262-265.
76. Tanaka, C., Sakuma, R., Nakamura, T., Hamada, H. and Saijoh, Y. (2007) Long-range action of Nodal requires interaction with GDF1. Genes Dev., 21, 3272-3282.
77. Shioda, T., Lechleider, R.J., Dunwoodie, S.L., Li, H., Yahata, T., de Caestecker, M.P., Fenner, M.H., Roberts, A.B. and Isselbacher, K.J. (1998) Transcriptional activating activity of Smad4: roles of SMAD hetero-oligomerization and enhancement by an associating transactivator. Proc. Natl Acad. Sci. USA, 95, 9785-9790.
78. Plisov, S., Tsang, M., Shi, G., Boyle, S., Yoshino, K., Dunwoodie, S.L., Dawid, I.B., Shioda, T., Perantoni, A.O. and de Caestecker, M.P. (2005) Cited1 is a bifunctional transcriptional cofactor that regulates early nephronic patterning. J. Am. Soc. Nephrol., 16, 1632-1644.
79. Schwenk, F., Baron, U. and Rajewsky, K. (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res., 23, 5080-5081.
80. Lowe, L.A., Yamada, S. and Kuehn, M.R. (2001) Genetic dissection of nodal function in patterning the mouse embryo. Development, 128, 1831-1843.
81. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
82. Tremblay, K.D., Dunn, N.R. and Robertson, E.J. (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development, 128, 3609-3621.
83. Dunwoodie, S.L., Henrique, D., Harrison, S.M. and Beddington, R.S. (1997) Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development, 124, 3065-3076.
84. Hogan, B., Beddington, R., Costantini, F. and Lacey, E. (1994) Manipulating the Mouse Embyo; A Laboratory Manual. Cold Spring Harbour Laboratory Press.
85. Kaufman, M.H. (1992) The Atlas of Mouse Development. Academic Press, London.
86. Rodriguez, T.A., Sparrow, D.B., Scott, A.N., Withington, S.L., Preis, J.I., Michalicek, J., Clements, M., Tsang, T.E., Shioda, T., Beddington, R.S. et al. (2004) Cited1 is required in trophoblasts for placental development and for embryo growth and survival. Mol. Cell. Biol., 24, 228-244.
87. Neidhardt, L.M., Kispert, A. and Herrmann, B.G. (1997) A mouse gene of the paired-related homeobox class expressed in the caudal somite compartment and in the developing vertebral column, kidney and nervous system. Dev. Genes Evol., 207, 330-339.
88. Sparrow, D.B., Guillen-Navarro, E., Fatkin, D. and Dunwoodie, S.L. (2008) Mutation of Hairy-and-Enhancer-of-Split-7 in humans causes spondylocostal dysostosis. Hum. Mol. Genet., 17, 3761-3766.
89. Umesono, K., Murakami, K.K., Thompson, C.C. and Evans, R.M. (1991) Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell, 65, 1255-1266.
90. Nikolova, V., Leimena, C., McMahon, A.C., Tan, J.C., Chandar, S., Jogia, D., Kesteven, S.H., Michalicek, J., Otway, R., Verheyen, F. et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J. Clin. Invest., 113, 357-369.