Loss-of-function of Gli3 in mice causes abnormal frontal bone morphology and premature synostosis of the interfrontal suture

Frontiers in Physiology

Volumn 3 MAY, Issue , 2012, Pages

  Veistinen, Lotta ^a,b   Takatalo, Maarit ^a   Tanimoto, Yukiho ^a   Kesper, Dörthe A ^c   Vortkamp, Andrea ^c   Rice, David P C ^a,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Finnish Graduate School of Oral Sciences   (Finland)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Bone; Craniosynostosis; Developmental biology; Gli3; Suture

Indexed keywords

EID: 84866385993     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00121     Document Type: Article

References (40)

1. Aberg, T., Rice, R., Rice, D., Thesleff, I., and Waltimo-Siren, J. (2005). Chon-drogenic potential of mouse cal-varial mesenchyme. J. Histochem. Cytochem. 53, 653-663.
2. Abzhanov, A., Rodda, S. J., McMahon, A. P., and Tabin, C. J. (2007). Regulation of skeletogenic differentiation in cranial dermal bone. Development 134,3133-3144.
3. Aldridge, K., Hill, C. A., Austin, J. R., Per-cival, C., Martinez-Abadias, N., Neu-berger, T., Wang, Y., Jabs, E. W., and Richtsmeier, J. T. (2010). Brain phe-notypes in two FGFR2 mouse models for Apert syndrome. Dev. Dyn. 239, 987-997.
4. Aoto, K., Nishimura, T., Eto, K., and Motoyama, J. (2002). Mouse GLI3 regulates Fgf8 expression and apop-tosis in the developing neural tube, face, and limb bud. Dev. Biol. 251, 320-332.
5. Blaess, S., Stephen, D., and Joyner, A. L. (2008). Gli3 coordinates three-dimensional patterning and growth of the tectum and cerebellum by integrating Shh and Fgf8 signaling. Development 135, 2093-2103.
6. Bradley, J. P., Levine, J. P., McCarthy, J. G., and Longaker, M. T. (1997). Studies in cranial suture biology: regional dura mater determines in vitro cranial suture fusion. Plast. Reconstr. Surg. 100, 1091-9; discussion 1100-1102.
7. Buscher, D., Grotewold, L., and Ruther, U. (1998). The XtJ allele generates a Gli3 fusion transcript. Mamm. Genome 9, 676-678.
8. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H., and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383, 407-413.
9. Gagan, J. R., Tholpady, S. S., and Ogle, R. C. (2007). Cellular dynamics and tissue interactions of the dura mater during head development. Birth Defects Res. C Embryo Today 81,297-304.
10. Huang, X., Goudy, S. L., Ketova, T., Litingtung, Y., and Chiang, C. (2008). Gli3-deficient mice exhibit cleft palate associated with abnormal tongue development. Dev. Dyn. 237, 3079-3087.
11. 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.
12. Hurst, J. A., Jenkins, D., Vasudevan, P. C., Kirchhoff, M., Skovby, F., Rieubland, C., Gallati, S., Rittinger, O., Kroisel, P. M., Johnson, D., Biesecker, L. G., and Wilkie, A. O. (2011). Metopic and sagittal synos-tosis in Greig cephalopolysyndactyly syndrome: five cases with intragenic mutations or complete deletions of GLI3. Eur. J. Hum. Genet. 19, 757-762.
13. Ishii, M., Merrill, A. E., Chan, Y. S., Gitel-man, I., Rice, D. P., Sucov, H. M., and Maxson, R. E. Jr. (2003). Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development 130,6131-6142.
14. Jeong, J., Mao, J., Tenzen, T., Kottmann, A. H., and McMahon, A. P. (2004). Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev. 18, 937-951.
15. Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M., and Morriss-Kay, G. M. (2002). Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241, 106-116.
16. Johnson, D. R. (1967). Extra-toes: anew mutant gene causing multiple abnormalities in the mouse. J. Embryol. Exp. Morphol. 17, 543-581.
17. Koziel, L., Wuelling, M., Schneider, S., and Vortkamp, A. (2005). Gli3 acts as a repressor downstream of Ihh in regulating two distinct steps of chondrocyte differentiation. Development 132,5249-5260.
18. Lenton, K., James, A. W., Manu, A., Brugmann, S. A., Birker, D., Nelson, E. R., Leucht, P., Helms, J. A., and Longaker, M. T. (2011). Indian hedgehog positively regulates cal-varial ossification and modulates bone morphogenetic protein signaling. Genesis 49, 784-796.
19. Litingtung, Y., Dahn, R. D., Li, Y., Fal-lon, 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.
20. Maynard, T. M., Jain, M. D., Balmer, C. W., and LaMantia, A. S. (2002). High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm. Genome 13,58-61.
21. McDonald-McGinn, D. M., Feret, H., Nah, H. D., Bartlett, S. P., Whitaker, L. A., and Zackai, E. H. (2010). Metopic craniosynostosis due to mutations in GLI3: a novel association. Am. J. Med. Genet. A 152A, 1654-1660.
22. Opperman, L. A., Sweeney, T. M., Red-mon, J., Persing, J. A., and Ogle, R. C. (1993). Tissue interactions with underlying dura mater inhibit osseous obliteration of developing cranial sutures. Dev. Dyn. 198, 312-322.
23. Pritchard, J. J., Scott, J. H., and Girgis, E G. (1956). The structure and development of cranial and facial sutures. J. Anat. 90, 73-86.
24. Rice, D. P., Aberg, T., Chan, Y., Tang, Z., Kettunen, P. J., Pakarinen, L., Maxson, R. E., and Thesleff, I. (2000). Integration of FGF and TWIST in calvarial bone and suture development. Development 127, 1845-1855.
25. Rice, D. P., Connor, E. C., Veltmaat, J. M.,Lana-Elola, E.,Veistinen,L.,Tan-imoto, Y., Bellusci, S., and Rice, R. (2010). Gli3Xt-J/Xt-J mice exhibit lambdoid suture craniosynostosis which results from altered osteo-progenitor proliferation and differentiation. Hum. Mol. Genet. 19, 3457-3467.
26. Rice, D. P., Kim, H. J., and Thesleff, I. (1999). Apoptosis in murine calvarial bone and suture development. Eur. J. Oral Sci. 107, 265-275.
27. Rice, D. P., Rice, R., and Thesleff, I. (2003a). Molecular mechanisms in calvarial bone and suture development, and their relation to craniosynostosis. Eur. J. Orthod. 25, 139-148.
28. Rice, R., Rice, D. P., Olsen, B. R., and Thesleff, I. (2003b). Progression of calvarial bone development requires Foxc1 regulation of Msx2 and Alx4. Dev. Biol. 262, 75-87.
29. Richtsmeier, J. T., Aldridge, K., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., Yan, P., and Cole, T. M. III. (2006). Phenotypic integration of neurocranium and brain. J. Exp. Zool. B Mol. Dev. Evol. 306, 360-378.
30. Roth, D. A., Bradley, J. P., Levine, J. P., McMullen, H. F., McCarthy, J. G., and Longaker, M. T. (1996). Studies in cranial suture biology: part II. Role of the dura in cranial suture fusion. Plast. Reconstr. Surg. 97, 693-699.
31. Sahar, D. E., Longaker, M. T., and Quarto, N. (2005). Sox9 neural crest determinant gene controls patterning and closure of the posterior frontal cranial suture. Dev. Biol. 280, 344-361.
32. Schowing, J. (1968). Demonstration of the inductive role of the brain in osteogenesis of the embryonic skull of the chicken. J. Embryol. Exp. Morphol. 19, 83-94.
33. Solem, R. C., Eames, B. F., Tokita, M., and Schneider, R. A. (2011). Mesenchymal and mechanical mechanisms of secondary cartilage induction. Dev. Biol. 356, 28-39.
34. St-Jacques, B., Hammerschmidt, M., and McMahon, A. P. (1999). Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13, 2072-2086
35. te Welscher, P., Zuniga, A., Kuijper, S., Drenth, T., Goedemans, H. J., Mei-jlink, F., and Zeller, R. (2002). Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298, 827-830.
36. Tole, S., Ragsdale, C. W., and Grove, E. A. (2000). Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev. Biol. 217, 254-265.
37. Vortkamp, A., Franz, T., Gessler, M., and Grzeschik, K. H. (1992). Deletion of GLI3 supports the homology of the human Greig cephalopolysyndactyly syndrome (GCPS) and the mouse mutant extra toes (Xt). Mamm. Genome 3, 461-463.
38. Vortkamp, A., Gessler, M., and Grzeschik, K. H. (1991). GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature 352, 539-540.
39. 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.
40. Wang, Y., Xiao, R., Yang, F., Karim, B. O., Iacovelli, A. J., Cai, J., Lerner, C. P., Richtsmeier, J. T., Leszl, J. M., Hill, C. A., Yu, K., Ornitz, D. M., Elisseeff, J., Huso, D. L., and Wang Jabs, E. (2005). Abnormalities in cartilage and bone develop ment in the Apert syndrome FGFR2(+/S252W) mouse. Development 132, 3537-3548.