Preaxial polydactyly caused by Gli3 haploinsufficiency is rescued by Zic3 loss of function in mice

Human Molecular Genetics

Volumn 21, Issue 8, 2012, Pages 1888-1896

  Quinn, Malgorzata E ^a   Haaning, Allison ^a   Ware, Stephanie M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI3; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE OVEREXPRESSION; HAPLOINSUFFICIENCY; HELA CELL; HETEROZYGOSITY; IN VITRO STUDY; LIMB DEVELOPMENT; LOSS OF FUNCTION MUTATION; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; POLYDACTYLY; PRIORITY JOURNAL; PROTEIN PROCESSING; REPRESSOR GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BODY PATTERNING; EMBRYO, MAMMALIAN; FORELIMB; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAPLOINSUFFICIENCY; HEDGEHOG PROTEINS; HINDLIMB; HOMEODOMAIN PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIMB BUDS; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; POLYDACTYLY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

ANIMALIA; ERINACEIDAE; MUS;

EID: 84859224287     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds002     Document Type: Article

References (45)

1. Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M. and Mikoshiba, K. (1994) A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem., 63, 1880-1890.
2. Nagai, T., Aruga, J., Takada, S., Gunther, T., Sporle, R., Schughart, K. and Mikoshiba, K. (1997) The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol., 182, 299-313.
3. Brown, S.A., Warburton, D., Brown, L.Y., Yu, C.Y., Roeder, E.R., Stengel-Rutkowski, S., Hennekam, R.C. and Muenke, M. (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat. Genet., 20, 180-183.
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. Vortkamp, A., Gessler, M. and Grzeschik, K.H. (1991) GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature, 352, 539-540.
6. Grinberg, I. and Millen, K.J. (2005) The ZIC gene family in development and disease. Clin. Genet., 67, 290-296.
7. Grinberg, I., Northrup, H., Ardinger, H., Prasad, C., Dobyns, W.B. and Millen, K.J. (2004) Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat. Genet., 36, 1053-1055.
8. 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.
9. Ahn, S. and Joyner, A.L. (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell, 118, 505-516.
10. Litingtung, Y., Dahn, R.D., Li, Y., Fallon, J.F. and Chiang, C. (2002) Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature, 418, 979-983.
11. Masuya, H., Sagai, T., Wakana, S., Moriwaki, K. and Shiroishi, T. (1995) A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev., 9, 1645-1653.
12. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999) Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem., 274, 8143-8152.
13. te Welscher, P., Zuniga, A., Kuijper, S., Drenth, T., Goedemans, H.J., Meijlink, F. and Zeller, R. (2002) Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science, 298, 827-830.
14. Zeller, R., Lopez-Rios, J. and Zuniga, A. (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet., 10, 845-858.
15. Wang, B., Fallon, J.F. and Beachy, P.A. (2000) Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell, 100, 423-434.
16. Buscher, D., Bosse, B., Heymer, J. and Ruther, U. (1997) Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mech. Dev., 62, 175-182.
17. Bastida, M.F., Delgado, M.D., Wang, B., Fallon, J.F., Fernandez-Teran, M. and Ros, M.A. (2004) Levels of Gli3 repressor correlate with Bmp4 expression and apoptosis during limb development. Dev. Dyn., 231, 148-160.
18. Davenport, T.G., Jerome-Majewska, L.A. and Papaioannou, V.E. (2003) Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development, 130, 2263-2273.
19. Galli, A., Robay, D., Osterwalder, M., Bao, X., Benazet, J.D., Tariq, M., Paro, R., Mackem, S. and Zeller, R. (2010) Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet., 6, e1000901.
20. Laufer, E., Nelson, C.E., Johnson, R.L., Morgan, B.A. and Tabin, C. (1994) Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell, 79, 993-1003.
21. Niswander, L., Jeffrey, S., Martin, G.R. and Tickle, C. (1994) A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature, 371, 609-612.
22. Qu, S., Niswender, K.D., Ji, Q., van der Meer, R., Keeney, D., Magnuson, M.A. and Wisdom, R. (1997) Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development, 124, 3999-4008.
23. Hui, C.C. and Joyner, A.L. (1993) A mouse model of Greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet., 3, 241-246.
24. Chiang, C., Litingtung, Y., Harris, M.P., Simandl, B.K., Li, Y., Beachy, P.A. and Fallon, J.F. (2001) Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol., 236, 421-435.
25. Kinzler, K.W. and Vogelstein, B. (1990) The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol., 10, 634-642.
26. 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.
27. 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.
28. 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.
29. Kang, S., Graham, J.M. Jr., Olney, A.H. and Biesecker, L.G. (1997) GLI3 frameshift mutations cause autosomal dominant Pallister-Hall syndrome. Nat. Genet., 15, 266-268.
30. 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.
31. 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.
32. Babbs, C., Furniss, D., Morriss-Kay, G.M. and Wilkie, A.O. (2008) Polydactyly in the mouse mutant Doublefoot involves altered Gli3 processing and is caused by a large deletion in cis to Indian hedgehog. Mech. Dev., 125, 517-526.
33. Sanz-Ezquerro, J.J. and Tickle, C. (2000) Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development. Development, 127, 4811-4823.
34. Amano, T., Sagai, T., Tanabe, H., Mizushina, Y., Nakazawa, H. and Shiroishi, T. (2009) Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev. Cell, 16, 47-57.
35. Harfe, B.D., Scherz, P.J., Nissim, S., Tian, H., McMahon, A.P. and Tabin, C.J. (2004) Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell, 118, 517-528.
36. Barna, M., Pandolfi, P.P. and Niswander, L. (2005) Gli3 and Plzf cooperate in proximal limb patterning at early stages of limb development. Nature, 436, 277-281.
37. Chen, Y., Knezevic, V., Ervin, V., Hutson, R., Ward, Y. and Mackem, S. (2004) Direct interaction with Hoxd proteins reverses Gli3-repressor function to promote digit formation downstream of Shh. Development, 131, 2339-2347.
38. Furushima, K., Murata, T., Matsuo, I. and Aizawa, S. (2000) A new murine zinc finger gene, Opr. Mech. Dev., 98, 161-164.
39. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G. and Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl Acad. Sci. USA, 97, 5978-5983.
40. Echelard, Y., Epstein, D.J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J.A. and McMahon, A.P. (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell, 75, 1417-1430.
41. Hui, C.C., Slusarski, D., Platt, K.A., Holmgren, R. and Joyner, A.L. (1994) Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol., 162, 402-413.
42. Kochhar, D.M. (1973) Limb development in mouse embryos. I. Analysis of teratogenic effects of retinoic acid. Teratology, 7, 289-298.
43. Kogerman, P., Grimm, T., Kogerman, L., Krause, D., Unden, A.B., Sandstedt, B., Toftgard, R. and Zaphiropoulos, P.G. (1999) Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat. Cell. Biol., 1, 312-319.
44. Shin, S.H., Kogerman, P., Lindstrom, E., Toftgard, R. and Biesecker, L.G. (1999) GLI3 mutations in human disorders mimic Drosophila cubitus interruptus protein functions and localization. Proc. Natl Acad. Sci. USA, 96, 2880-2884.
45. Patton, J.T. and Kaufman, M.H. (1995) The timing of ossification of the limb bones, and growth rates of various long bones of the fore and hind limbs of the prenatal and early postnatal laboratory mouse. J. Anat., 186, 175-185