Cis-regulatory underpinnings of human GLI3 expression in embryonic craniofacial structures and internal organs

Development Growth and Differentiation

Volumn 55, Issue 8, 2013, Pages 699-709

  Abbasi, Amir A ^a   Minhas, Rashid ^a   Schmidt, Ansgar ^b   Koch, Sabine ^b   Grzeschik, Karl Heinz ^b  

^a QUAID I AZAM UNIVERSITY   (Pakistan)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Conserved non coding elements; Enhancer; GLI3 expression; Transgenic mice; Zebrafish

Indexed keywords

CIS ACTING ELEMENT; TRANSCRIPTION FACTOR GLI3;

ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENHANCER REGION; EYE; GENE EXPRESSION; INTESTINE; INTRON; LIMB; MOUSE; NONHUMAN; REPORTER GENE; SEQUENCE ANALYSIS; TRANSGENIC MOUSE; UROGENITAL SYSTEM; ZEBRA FISH;

DANIO RERIO; ERINACEIDAE; MAMMALIA; MUS MUSCULUS; VERTEBRATA;

CONSERVED NON-CODING ELEMENTS; ENHANCER; GLI3 EXPRESSION; TRANSGENIC MICE; ZEBRAFISH;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTRONS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURAL TUBE; ORGAN SPECIFICITY; ORGANOGENESIS; SKULL; TRANSCRIPTION, GENETIC;

EID: 84885844994     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12076     Document Type: Article

References (58)

1. Abbasi, A. A. 2010. Unraveling ancient segmental duplication events in human genome by phylogenetic analysis of multigene families residing on HOX-cluster paralogons. Mol. Phylogenet. Evol. 57, 836-848.
2. Abbasi, A. A. 2011. Evolution of vertebrate appendicular structures: insight from genetic and palaeontological data. Dev. Dyn. 240, 1005-1016.
3. Abbasi, A. A., Goode, D. K., Amir, S. & Grzeschik, K. H. 2009. Evolution and functional diversification of the GLI family of transcription factors in vertebrates. Evol. Bioinform. Online 5, 5-13.
4. Abbasi, A. A., Paparidis, Z., Malik, S., Bangs, F., Schmidt, A., Koch, S., Lopez-Rios, J. & Grzeschik, K. H. 2010. Human intronic enhancers control distinct sub-domains of Gli3 expression during mouse CNS and limb development. BMC Dev. Biol. 10, 44.
5. Abbasi, A. A., Paparidis, Z., Malik, S., Goode, D. K., Callaway, H., Elgar, G. & Grzeschik, K. H. 2007. Human GLI3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS One 2, e366.
6. Alvarez-Medina, R., Cayuso, J., Okubo, T., Takada, S. & Marti, E. 2008. Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development 135, 237-247.
7. Anderson, E., Peluso, S., Lettice, L. A. & Hill, R. E. 2012. Human limb abnormalities caused by disruption of hedgehog signaling. Trends Genet. 28, 364-373.
8. 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.
9. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D. & Joyner, A. L. 2002. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761.
10. Bai, C. B. & Joyner, A. L. 2001. Gli1 can rescue the in vivo function of Gli2. Development 128, 5161-5172.
11. Bai, C. B., Stephen, D. & Joyner, A. L. 2004. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 6, 103-115.
12. Biesecker, L. G. & Ondrey, F. 1998. Pallister-Hall syndrome. Otolaryngol. Head Neck Surg. 119, 556.
13. Bose, J., Grotewold, L. & Ruther, U. 2002. Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum. Mol. Genet. 11, 1129-1135.
14. Brewster, R., Mullor, J. L. & Ruiz i Altaba, A. 2000. Gli2 functions in FGF signaling during antero-posterior patterning. Development 127, 4395-4405.
15. Brudno, M., Do, C. B., Cooper, G. M., Kim, M. F. & Davydov, E. J. 2003. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 13, 721-731.
16. Buttitta, L., Mo, R., Hui, C. C. & Fan, C. M. 2003. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 130, 6233-6243.
17. Corrales, J. D., Rocco, G. L., Blaess, S., Guo, Q. & Joyner, A. L. 2004. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131, 5581-5590.
18. Couly, G., Grapin-Botton, A., Coltey, P., Ruhin, B. & Le Douarin, N. M. 1998. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125, 3445-3459.
19. Coy, S., Caamano, J. H., Carvajal, J., Cleary, M. L. & Borycki, A. G. 2011. A novel Gli3 enhancer controls the Gli3 spatiotemporal expression pattern through a TALE homeodomain protein binding site. Mol. Cell. Biol. 31, 1432-1443.
20. Ding, Q., Motoyama, J., Gasca, S., Mo, R., Sasaki, H., Rossant, J. & Hui, C. C. 1998. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125, 2533-2543.
21. Franz, T. & Besecke, A. 1991. The development of the eye in homozygotes of the mouse mutant Extra-toes. Anat. Embryol. (Berl) 184, 355-361.
22. Furimsky, M. & Wallace, V. A. 2006. Complementary Gli activity mediates early patterning of the mouse visual system. Dev. Dyn. 235, 594-605.
23. Haraguchi, R., Mo, R., Hui, C., Motoyama, J., Makino, S., Shiroishi, T., Gaffield, W. & Yamada, G. 2001. Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128, 4241-4250.
24. Hardcastle, Z., Mo, R., Hui, C. C. & Sharpe, P. T. 1998. The Shh signalling pathway in tooth development: defects in Gli2 and Gli3 mutants. Development 125, 2803-2811.
25. Hatsell, S. J. & Cowin, P. 2006. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development 133, 3661-3670.
26. Hu, M. C., Mo, R., Bhella, S., Wilson, C. W., Chuang, P. T., Hui, C. C. & Rosenblum, N. D. 2006. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133, 569-578.
27. Hui, C. C. & 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.
28. Johnson, D. R. 1967. Extra-toes: anew mutant gene causing multiple abnormalities in the mouse. J. Embryol. Exp. Morphol. 17, 543-581.
29. Kalff-Suske, M., Wild, A., Topp, J., Wessling, M., Jacobsen, E. M., Bornholdt, D., Engel, H., Heuer, H., Aalfs, C. M., Ausems, M. G., Barone, R., Herzog, A., Heutink, P., Homfray, T., Gillessen-Kaesbach, G., Konig, R., Kunze, J., Meinecke, P., Muller, D., Rizzo, R., Strenge, S., Superti-Furga, A. & Grzeschik, K. H. 1999. Point mutations throughout the GLI3 gene cause Greig cephalopolysyndactyly syndrome. Hum. Mol. Genet. 8, 1769-1777.
30. Kang, S., Allen, J., Graham, J. M. Jr, Grebe, T., Clericuzio, C., Patronas, N., Ondrey, F., Green, E., Schaffer, A., Abbott, M. & Biesecker, L. G. 1997a. Linkage mapping and phenotypic analysis of autosomal dominant Pallister-Hall syndrome. J. Med. Genet. 34, 441-446.
31. Kang, S., Graham, J. M. Jr, Olney, A. H. & Biesecker, L. G. 1997b. GLI3 frameshift mutations cause autosomal dominant Pallister-Hall syndrome. Nat. Genet. 15, 266-268.
32. Kim, J. H., Huang, Z. & Mo, R. 2005. Gli3 null mice display glandular overgrowth of the developing stomach. Dev. Dyn. 234, 984-991.
33. Koziel, L., Wuelling, M., Schneider, S. & Vortkamp, A. 2005. Gli3 acts as a repressor downstream of Ihh in regulating two distinct steps of chondrocyte differentiation. Development 132, 5249-5260.
34. Kuschel, S., Ruther, U. & Theil, T. 2003. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev. Biol. 260, 484-495.
35. Matise, M. P., Epstein, D. J., Park, H. L., Platt, K. A. & Joyner, A. L. 1998. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770.
36. Mayor, C., Brudno, M., Schwartz, J. R., Poliakov, A., Rubin, E. M., Frazer, K. A., Pachter, L. S. & Dubchak, I. 2000. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16, 1046-1047.
37. McDermott, A., Gustafsson, M., Elsam, T., Hui, C. C., Emerson, C. P. Jr & Borycki, A. G. 2005. Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132, 345-357.
38. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H., Joyner, A. L. & Hui, C. 1997. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123.
39. Motoyama, J., Liu, J., Mo, R., Ding, Q., Post, M. & Hui, C. C. 1998. Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat. Genet. 20, 54-57.
40. Noden, D. M. 1983. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev. Biol. 96, 144-165.
41. Paparidis, Z., Abbasi, A. A., Malik, S., Goode, D. K., Callaway, H., Elgar, G., deGraaff, E., Lopez-Rios, J., Zeller, R. & Grzeschik, K. H. 2007. Ultraconserved non-coding sequence element controls a subset of spatiotemporal GLI3 expression. Dev. Growth Differ. 49, 543-553.
42. Persson, M., Stamataki, D., te Welscher, P., Andersson, E., Bose, J., Ruther, U., Ericson, J. & Briscoe, J. 2002. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16, 2865-2878.
43. Pohl, T. M., Mattei, M. G. & Ruther, U. 1990. Evidence for allelism of the recessive insertional mutation add and the dominant mouse mutation extra-toes (Xt). Development 110, 1153-1157.
44. Pu, Y., Huang, L. & Prins, G. S. 2004. Sonic hedgehog-patched Gli signaling in the developing rat prostate gland: lobe-specific suppression by neonatal estrogens reduces ductal growth and branching. Dev. Biol. 273, 257-275.
45. Radhakrishna, U., Bornholdt, D., Scott, H. S., Patel, U. C., Rossier, C., Engel, H., Bottani, A., Chandal, D., Blouin, J. L., Solanki, J. V., Grzeschik, K. H. & Antonarakis, S. E. 1999. The phenotypic spectrum of GLI3 morphopathies includes autosomal dominant preaxial polydactyly type-IV and postaxial polydactyly type-A/B; No phenotype prediction from the position of GLI3 mutations. Am. J. Hum. Genet. 65, 645-655.
46. Radhakrishna, U., Wild, A., Grzeschik, K. H. & Antonarakis, S. E. 1997. Mutation in GLI3 in postaxial polydactyly type A. Nat. Genet. 17, 269-271.
47. Rallu, M., Corbin, J. G. & Fishell, G. 2002. Parsing the prosencephalon. Nat. Rev. Neurosci. 3, 943-951.
48. Robert, B. & Lallemand, Y. 2006. Anteroposterior patterning in the limb and digit specification: contribution of mouse genetics. Dev. Dyn. 235, 2337-2352.
49. Ruiz i Altaba, A., Nguyen, V. & Palma, V. 2003. The emergent design of the neural tube: prepattern, SHH morphogen and GLI code. Curr. Opin. Genet. Dev. 13, 513-521.
50. Schimmang, T., Lemaistre, M., Vortkamp, A. & Ruther, U. 1992. Expression of the zinc finger gene Gli3 is affected in the morphogenetic mouse mutant extra-toes (Xt). Development 116, 799-804.
51. Schimmang, T., Oda, S. I. & Ruther, U. 1994. The mouse mutant Polydactyly Nagoya (Pdn) defines a novel allele of the zinc finger gene Gli3. Mamm. Genome 5, 384-386.
52. Tyurina, O. V., Guner, B., Popova, E., Feng, J., Schier, A. F., Kohtz, J. D. & Karlstrom, R. O. 2005. Zebrafish Gli3 functions as both an activator and a repressor in Hedgehog signaling. Dev. Biol. 277, 537-556.
53. Veltmaat, J. M., Relaix, F., Le, L. T., Kratochwil, K., Sala, F. G., van Veelen, W., Rice, R., Spencer-Dene, B., Mailleux, A. A., Rice, D. P., Thiery, J. P. & Bellusci, S. 2006. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development 133, 2325-2335.
54. Verloes, A., David, A., Ngo, L. & Bottani, A. 1995. Stringent delineation of Pallister-Hall syndrome in two long surviving patients: importance of radiological anomalies of the hands. J. Med. Genet. 32, 605-611.
55. Vortkamp, A., Gessler, M. & Grzeschik, K. H. 1991. GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature 352, 539-540.
56. Wijgerde, M., McMahon, J. A., Rule, M. & McMahon, A. P. 2002. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 16, 2849-2864.
57. Wild, A., Kalff-Suske, M., Vortkamp, A., Bornholdt, D., Konig, R. & Grzeschik, K. H. 1997. Point mutations in human GLI3 cause Greig syndrome. Hum. Mol. Genet. 6, 1979-1984.
58. Zaki, P. A., Collinson, J. M., Toraiwa, J., Simpson, T. I., Price, D. J. & Quinn, J. C. 2006. Penetrance of eye defects in mice heterozygous for mutation of Gli3 is enhanced by heterozygous mutation of Pax6. BMC Dev. Biol. 6, 46.