Direct interaction with Hoxd protein reverses Gli3-repressor function to promote digit formation downstream of Shh

Development

Volumn 131, Issue 10, 2004, Pages 2339-2347

  Chen, Yuting ^a   Knezevic, Vladimir ^a,b   Ervin, Valerie ^a   Hutson, Richard ^a,c   Ward, Yvona ^a   Mackem, Susan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b 20/20 GeneSystems Inc   (United States)

^c United States Patent and Trademark Office   (United States)

Author keywords

AP pattern; Digit formation; Gli3; Hoxd genes; Limb development; Mouse; Sonic hedgehog

Indexed keywords

HOX PROTEIN; HOXD PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; FINGER; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE REPRESSION; LIMB BUD; LIMB DEVELOPMENT; MOUSE; NONHUMAN; POLYDACTYLY; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CATTLE; CROSSES, GENETIC; DNA-BINDING PROTEINS; FEMALE; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MICE, INBRED C3H; MICE, INBRED STRAINS; MICE, KNOCKOUT; MORPHOGENESIS; NERVE TISSUE PROTEINS; POLYDACTYLY; REPRESSOR PROTEINS; TOES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

ANIMALIA; ERINACEIDAE;

EID: 3042756178     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01115     Document Type: Article

References (37)

1. Altaba, A. R. I. (1999). Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126, 3205-3216.
2. Biesecker, L. G. (1997). Strike three for GLI3. Nat. Genet. 17, 259-260.
3. Bose, J., Grotewold, L. and Ruther, U. (2002). Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum. Mol. Genet. 11, 1129-1135.
4. Buscher, D., Grotewold, L. and Ruther, U. (1998). The Xt(J) allele generates a Gli3 fusion transcript. Mamm. Genome 9, 676-678.
5. 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.
6. Dahn, R. D. and Fallon, J. F. (2000). Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289, 438-441.
7. 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.
8. DiRocco, G., Mavilio, F. and Zappavigna, V. (1997). Functional dissection of a transcriptionally active, target-specific Hox-Pbx complex. EMBO J. 16, 3644-3654.
9. Dolle, P., Izpisua-Belmonte, J. C., Falkenstein, H., Renucci, A. and Duboule, D. (1989). Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern-formation. Nature 342, 767-772.
10. Fromental-Ramain, C., Warot, X., Messadecq, N., LeMeur, M., Dolle, P. and Chambon, P. (1996). Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011.
11. Goff, D. J. and Tabin, C. J. (1997). Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. Development 124, 627-636.
12. Goodrich, L. V., Johnson, R. L., Milenkovic, L., McMahon, J. A. and Scott, M. P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 10, 301-312.
13. Hui, C. C. and Joyner, A. L. (1993). A mouse model of Greig cephalapolysyndactyly syndrome: the extra-toes' mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3, 241-246.
14. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
15. Knezevic, V., De Santo, R., Schughart, K., Huffstadt, U., Chiang, C., Mahon, K. A. and Mackem, S. (1997). Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop. Development 124, 4523-4536.
16. Kraus, P., Fraidenraich, D. and Loomis, C. A. (2001). Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech. Dev. 100, 45-58.
17. Lewis, P. M., Dunn, M. P., McMahon, J. A., Logan, M., Martin, J. F., St-Jacques, B. and McMahon, A. P. (2001). Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell 105, 599-612.
18. Litingtung, Y., Dahn, R. D., Li, Y. N., 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.
19. Mariani, F. V. and Martin, G. R. (2003). Deciphering skeletal patterning: clues from the limb. Nature 423, 319-325.
20. Masuya, H., Sagai, T., Wakana, S., Moriwaki, K. and Shiroishi, T. A. (1995). Duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev. 9, 1645-1653.
21. Meyer, N. P. and Roelink, H. (2003). The amino-terminal region of Gli3 antagonizes the Shh response and acts in dorsoventral fate specification in the developing spinal cord. Dev. Biol. 257, 343-355.
22. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H. Q., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H., Joyner, A. L. and Hui, C. C. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123.
23. Morgan, B. A., Izpisua-Belmonte, J. C., Duboule, D. and Tabin, C. J. (1992). Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358, 236-239.
24. Nelson, C. E., Morgan, B. A., Burke, A. C., Laufer, E., DiMambro, E., Murtaugh, L. C., Gonzales, E., Tessarollo, L., Parada, L. F. and Tabin, C. (1996). Analysis of Hox gene expression in the chick limb bud. Development 122, 1449-1466.
25. Sasaki, H., Hui, C. C., Nakafuku, M. and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3 beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322.
26. Schweitzer, R., Vogan, K. J. and Tabin, C. J. (2000). Similar expression and regulation of Gli2 and Gli3 in the chick limb bud. Mech. Dev. 98, 171-174.
27. 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.
28. Sordino, P., Vanderhoeven, F. and Duboule, D. (1995). Hox gene-expression in teleost fins and the origin of vertebrate digits. Nature 375, 678-681.
29. Storm, E. E. and Kingsley, D. M. (1996). Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122, 3969-3979.
30. te Weischer, P. T., 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.
31. Tickle, C. (2003). Patterning systems - from one end of the limb to the other. Dev. Cell 4, 449-458.
32. Wang, B. L., 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.
33. Wellik, D. M. and Capecchi, M. R. (2003). Hox10 and Hex11 genes are required to globally pattern the mammalian skeleton. Science 301, 363-367.
34. Yang, Y., Drossopoulou, G., Chuang, P. T., Duprez, D., Marti, E., Bumcrot, D., Vargesson, N., Clarke, J., Niswander, L., McMahon, A. and Tickle, C. (1997). Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124, 4393-4404.
35. Zakany, J. and Duboule, D. (1999). Hox genes in digit development and evolution. Cell Tissue Res. 296, 19-25.
36. Zakany, J., Fromental-Ramain, C., Warot, X. and Duboule, D. (1997). Regulation of number and size of digits by posterior Hox genes: a dose-dependent mechanism with potential evolutionary implications. Proc. Natl. Acad. Sci. USA 94, 13695-13700.
37. Zuniga, A. and Zeller, R. (1999). Gli3 (Xt) and formin (Id) participate in the positioning of the polarising region and control of posterior limb-bud identity. Development 126, 13-21.