Loss of tgif function causes holoprosencephaly by disrupting the Shh signaling pathway

PLoS Genetics

Volumn 8, Issue 2, 2012, Pages

  Taniguchi, Kenichiro ^a   Anderson, Anoush E ^a   Sutherland, Ann E ^a   Wotton, David ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; PROTEIN NODAL; SONIC HEDGEHOG PROTEIN; THYMINE GUANINE INTERACTING FACTOR 1; THYMINE GUANINE INTERACTING FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DISEASE SEVERITY; EMBRYO; EMBRYO PATTERN FORMATION; EYE MALFORMATION; FOREBRAIN; GENE; GENE MUTATION; HETEROZYGOSITY; HOLOPROSENCEPHALY; LOSS OF FUNCTION MUTATION; MOUSE; NEURAL TUBE; NONHUMAN; NOSE MALFORMATION; NULL ALLELE; PATHOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; SHH GENE; SIGNAL TRANSDUCTION; TGIF1 GENE; TGIF2 GENE; UPREGULATION;

ANIMALS; DISEASE MODELS, ANIMAL; GENES, HOMEOBOX; HEDGEHOG PROTEINS; HOLOPROSENCEPHALY; HOMEODOMAIN PROTEINS; HUMANS; MICE; MUTATION; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TGF-BETA SUPERFAMILY PROTEINS;

ERINACEIDAE; MUS;

EID: 84859177990     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002524     Document Type: Article

References (80)

1. Geng X, Oliver G, (2009) Pathogenesis of holoprosencephaly. J Clin Invest 119: 1403-1413.
2. Muenke M, Beachy PA, (2001) Holoprosencephaly. In: C.R. S, A.L. B, W.S. S, D. V, B. C, editors. The metabolic and molecular bases of inherited disease: McGraw-Hill pp. 6203-6230.
3. Leoncini E, Baranello G, Orioli IM, Anneren G, Bakker M, et al. (2008) Frequency of holoprosencephaly in the International Clearinghouse Birth Defects Surveillance Systems: searching for population variations. Birth Defects Res A Clin Mol Teratol 82: 585-591.
4. Matsunaga E, Shiota K, (1977) Holoprosencephaly in human embryos: epidemiologic studies of 150 cases. Teratology 16: 261-272.
5. Roach E, Demyer W, Conneally PM, Palmer C, Merritt AD, (1975) Holoprosencephaly: birth data, genetic and demographic analyses of 30 families. Birth Defects Orig Artic Ser 11: 294-313.
6. Rubenstein JL, Beachy PA, (1998) Patterning of the embryonic forebrain. Curr Opin Neurobiol 8: 18-26.
7. Golden JA, (1998) Holoprosencephaly: a defect in brain patterning. J Neuropathol Exp Neurol 57: 991-999.
8. Olsen CL, Hughes JP, Youngblood LG, Sharpe-Stimac M, (1997) Epidemiology of holoprosencephaly and phenotypic characteristics of affected children: New York State, 1984-1989. Am J Med Genet 73: 217-226.
9. Croen LA, Shaw GM, Lammer EJ, (1996) Holoprosencephaly: epidemiologic and clinical characteristics of a California population. Am J Med Genet 64: 465-472.
10. Roessler E, Muenke M, (1998) Holoprosencephaly: a paradigm for the complex genetics of brain development. J Inherit Metab Dis 21: 481-497.
11. Wallis DE, Muenke M, (1999) Molecular Mechanisms of Holoprosencephaly. Mol Genet Metab 68: 126-138.
12. Muenke M, Beachy PA, (2000) Genetics of ventral forebrain development and holoprosencephaly. Curr Opin Genet Dev 10: 262-269.
13. Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, et al. (1996) Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 14: 357-360.
14. Roessler E, Belloni E, Gaudenz K, Vargas F, Scherer SW, et al. (1997) Mutations in the C-terminal domain of Sonic Hedgehog cause holoprosencephaly. Hum Mol Genet 6: 1847-1853.
15. Nanni L, Ming JE, Bocian M, Steinhaus K, Bianchi DW, et al. (1999) The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly. Hum Mol Genet 8: 2479-2488.
16. Roessler E, Ward DE, Gaudenz K, Belloni E, Scherer SW, et al. (1997) Cytogenetic rearrangements involving the loss of the Sonic Hedgehog gene at 7q36 cause holoprosencephaly. Hum Genet 100: 172-181.
17. Gurrieri F, Trask BJ, van den Engh G, Krauss CM, Schinzel A, et al. (1993) Physical mapping of the holoprosencephaly critical region on chromosome 7q36. Nat Genet 3: 247-251.
18. Wallis DE, Roessler E, Hehr U, Nanni L, Wiltshire T, et al. (1999) Mutations in the homeodomain of the human SIX3 gene cause holoprosencephaly. Nat Genet 22: 196-198.
19. Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, et al. (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20: 180-183.
20. Gripp KW, Wotton D, Edwards MC, Roessler E, Ades L, et al. (2000) Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination. Nat Genet 25: 205-208.
21. Geng X, Speirs C, Lagutin O, Inbal A, Liu W, et al. (2008) Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev Cell 15: 236-247.
22. Jeong Y, Leskow FC, El-Jaick K, Roessler E, Muenke M, et al. (2008) Regulation of a remote Shh forebrain enhancer by the Six3 homeoprotein. Nat Genet 40: 1348-1353.
23. Shimamura K, Rubenstein JL, (1997) Inductive interactions direct early regionalization of the mouse forebrain. Development 124: 2709-2718.
24. Aoto K, Nishimura T, Eto K, Motoyama J, (2002) Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 251: 320-332.
25. Fuccillo M, Joyner AL, Fishell G, (2006) Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci 7: 772-783.
26. Tole S, Ragsdale CW, Grove EA, (2000) Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev Biol 217: 254-265.
27. Rallu M, Machold R, Gaiano N, Corbin JG, McMahon AP, et al. (2002) Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 129: 4963-4974.
28. Hebert JM, Fishell G, (2008) The genetics of early telencephalon patterning: some assembly required. Nat Rev Neurosci 9: 678-685.
29. Gutin G, Fernandes M, Palazzolo L, Paek H, Yu K, et al. (2006) FGF signalling generates ventral telencephalic cells independently of SHH. Development 133: 2937-2946.
30. Bertolino E, Reimund B, Wildt-Perinic D, Clerc R, (1995) A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J Biol Chem 270: 31178-31188.
31. Wotton D, Lo RS, Lee S, Massague J, (1999) A Smad transcriptional corepressor. Cell 97: 29-39.
32. Heldin C-H, Miyazono K, ten Dijke P, (1997) TGF-ß signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471.
33. Massague J, Seoane J, Wotton D, (2005) Smad transcription factors. Genes Dev 19: 2783-2810.
34. Wotton D, Massague J, (2001) Smad transcriptional corepressors in TGF beta family signaling. Curr Top Microbiol Immunol 254: 145-164.
35. Imoto I, Pimkhaokham A, Watanabe T, Saito-Ohara F, Soeda E, et al. (2000) Amplification and overexpression of TGIF2, a novel homeobox gene of the TALE superclass, in ovarian cancer cell lines. Biochem Biophys Res Commun 276: 264-270.
36. Melhuish TA, Gallo CM, Wotton D, (2001) TGIF2 interacts with histone deacetylase 1 and represses transcription. J Biol Chem 276: 32109-32114.
37. Melhuish TA, Wotton D, (2006) The Tgif2 gene contains a retained intron within the coding sequence. BMC Mol Biol 7: 2.
38. Bartholin L, Powers SE, Melhuish TA, Lasse S, Weinstein M, et al. (2006) TGIF inhibits retinoid signaling. Mol Cell Biol 26: 990-1001.
39. Melhuish TA, Chung DD, Bjerke GA, Wotton D, (2010) Tgif1 represses apolipoprotein gene expression in liver. J Cell Biochem 111: 380-390.
40. Aguilella C, Dubourg C, Attia-Sobol J, Vigneron J, Blayau M, et al. (2003) Molecular screening of the TGIF gene in holoprosencephaly: identification of two novel mutations. Hum Genet 112: 131-134.
41. Chen CP, Chern SR, Du SH, Wang W, (2002) Molecular diagnosis of a novel heterozygous 268C→T (R90C) mutation in TGIF gene in a fetus with holoprosencephaly and premaxillary agenesis. Prenat Diagn 22: 5-7.
42. El-Jaick KB, Powers SE, Bartholin L, Myers KR, Hahn J, et al. (2007) Functional analysis of mutations in TGIF associated with holoprosencephaly. Mol Genet Metab 90: 97-111.
43. Jin JZ, Gu S, McKinney P, Ding J, (2006) Expression and functional analysis of Tgif during mouse midline development. Dev Dyn 235: 547-553.
44. Mar L, Hoodless PA, (2006) Embryonic fibroblasts from mice lacking Tgif were defective in cell cycling. Mol Cell Biol 26: 4302-4310.
45. Shen J, Walsh CA, (2005) Targeted disruption of Tgif, the mouse ortholog of a human holoprosencephaly gene, does not result in holoprosencephaly in mice. Mol Cell Biol 25: 3639-3647.
46. Bartholin L, Melhuish TA, Powers SE, Goddard-Leon S, Treilleux I, et al. (2008) Maternal Tgif is required for vascularization of the embryonic placenta. Dev Biol 319: 285-297.
47. Kuang C, Xiao Y, Yang L, Chen Q, Wang Z, et al. (2006) Intragenic deletion of Tgif causes defectsin brain development. Hum Mol Genet 15: 3508-3519.
48. Powers SE, Taniguchi K, Yen W, Melhuish TA, Shen J, et al. (2010) Tgif1 and Tgif2 regulate Nodal signaling and are required for gastrulation. Development 137: 249-259.
49. Hayashi S, Lewis P, Pevny L, McMahon AP, (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev 119 (Suppl 1): S97-S101.
50. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, et al. (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
51. Ma Y, Erkner A, Gong R, Yao S, Taipale J, et al. (2002) Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 111: 63-75.
52. Martynoga B, Morrison H, Price DJ, Mason JO, (2005) Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 283: 113-127.
53. Silvestri C, Narimatsu M, von Both I, Liu Y, Tan NB, et al. (2008) Genome-wide identification of Smad/Foxh1 targets reveals a role for Foxh1 in retinoic acid regulation and forebrain development. Dev Cell 14: 411-423.
54. Thomas P, Beddington R, (1996) Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr Biol 6: 1487-1496.
55. Fukuchi-Shimogori T, Grove EA, (2003) Emx2 patterns the neocortex by regulating FGF positional signaling. Nat Neurosci 6: 825-831.
56. Lewis SL, Tam PP, (2006) Definitive endoderm of the mouse embryo: formation, cell fates, and morphogenetic function. Dev Dyn 235: 2315-2329.
57. Martinez Barbera JP, Clements M, Thomas P, Rodriguez T, Meloy D, et al. (2000) The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127: 2433-2445.
58. Sasaki H, Hogan BL, (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118: 47-59.
59. Lewis SL, Khoo PL, Andrea De Young R, Bildsoe H, Wakamiya M, et al. (2007) Genetic interaction of Gsc and Dkk1 in head morphogenesis of the mouse. Mech Dev 124: 157-165.
60. Ingham PW, McMahon AP, (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15: 3059-3087.
61. Aoto K, Shikata Y, Imai H, Matsumaru D, Tokunaga T, et al. (2009) Mouse Shh is required for prechordal plate maintenance during brain and craniofacial morphogenesis. Dev Biol 327: 106-120.
62. Blaess S, Stephen D, Joyner AL, (2008) Gli3 coordinates three-dimensional patterning and growth of the tectum and cerebellum by integrating Shh and Fgf8 signaling. Development 135: 2093-2103.
63. Nomura M, Li E, (1998) Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393: 786-790.
64. Ohkubo Y, Chiang C, Rubenstein JL, (2002) Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111: 1-17.
65. Storm EE, Garel S, Borello U, Hebert JM, Martinez S, et al. (2006) Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133: 1831-1844.
66. Solomon BD, Mercier S, Velez JI, Pineda-Alvarez DE, Wyllie A, et al. (2010) Analysis of genotype-phenotype correlations in human holoprosencephaly. Am J Med Genet C Semin Med Genet 154C: 133-141.
67. Sanek NA, Taylor AA, Nyholm MK, Grinblat Y, (2009) Zebrafish zic2a patterns the forebrain through modulation of Hedgehog-activated gene expression. Development 136: 3791-3800.
68. Warr N, Powles-Glover N, Chappell A, Robson J, Norris D, et al. (2008) Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17: 2986-2996.
69. Hyman CA, Bartholin L, Newfeld SJ, Wotton D, (2003) Drosophila TGIF proteins are transcriptional activators. Mol Cell Biol 23: 9262-9274.
70. Lammer EJ, Chen DT, Hoar RM, Agnish ND, Benke PJ, et al. (1985) Retinoic acid embryopathy. N Engl J Med 313: 837-841.
71. Sulik KK, Dehart DB, Rogers JM, Chernoff N, (1995) Teratogenicity of low doses of all-trans retinoic acid in presomite mouse embryos. Teratology 51: 398-403.
72. De La Cruz JM, Bamford RN, Burdine RD, Roessler E, Barkovich AJ, et al. (2002) A loss-of-function mutation in the CFC domain of TDGF1 is associated with human forebrain defects. Hum Genet 110: 422-428.
73. Roessler E, Ouspenskaia MV, Karkera JD, Velez JI, Kantipong A, et al. (2008) Reduced NODAL signaling strength via mutation of several pathway members including FOXH1 is linked to human heart defects and holoprosencephaly. Am J Hum Genet 83: 18-29.
74. Ding J, Yang L, Yan YT, Chen A, Desai N, et al. (1998) Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395: 702-707.
75. Hoodless PA, Pye M, Chazaud C, Labbe E, Attisano L, et al. (2001) FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev 15: 1257-1271.
76. Collignon J, Varlet I, Robertson EJ, (1996) Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381: 155-158.
77. Ju W, Ogawa A, Heyer J, Nierhof D, Yu L, et al. (2006) Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation. Mol Cell Biol 26: 654-667.
78. Lewis PM, Dunn MP, McMahon JA, Logan M, Martin JF, et al. (2001) Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell 105: 599-612.
79. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, et al. (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52-54.
80. Wilkinson DG, (1992) In situ hybridization: a practical approach. pp. 75-83.