Protein kinase A antagonizes Hedgehog signaling by regulating both the activator and repressor forms of Cubitus interruptus

Genes and Development

Volumn 13, Issue 21, 1999, Pages 2828-2837

  Wang, Gelin ^a   Wang, Bing ^a   Jiang, Jin ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Ci; Hedgehog; Limb development; PKA; Proteolysis; Slimb

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; TRANSCRIPTION FACTOR;

ARTICLE; DROSOPHILA; ENZYME ACTIVATION; ENZYME REPRESSION; HEDGEHOG; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION;

ANIMALS; CELL CYCLE PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; INSECT PROTEINS; MUTAGENESIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES;

ANIMALIA; CUBITUS; CUBITUS INTERRUPTUS; ERINACEIDAE; HEXAPODA;

EID: 0032728958     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.21.2828     Document Type: Article

References (54)

1. Alcedo, J. and M. Noll. 1997. Hedgehog and its Patched-Smoothened receptor complex: a Novel signalling mechanism at the cell surface. Biol. Cenm. 378: 583-590.
2. Alcedo, J., M. Ayzenzon, T. Von Ohlen, M. Noll, and J.E. Hooper. 1996. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the Hedgehog signal. Cell 86: 231-232.
3. Alexandre, C., A. Jacinto, and P.W. Ingham. 1996. Transcriptional activation of Hedgehog target genes in Drosophila is mediated directly by the Cubitus interruptus protein, a member of the GLI family of the zinc finger DNA-binding proteins. Genes & Dev. 10: 2003-2013.
4. Alves, G., B. Limbourg-Bouchon, H. Tricoire, J. Brissard-Zahraoui, C. Lamour-Isnard, and D. Busson. 1998. Modulation of Hedgehog target gene expression by the Fused serine-threonine kinase in wing imaginal discs. Mech. Dev. 78: 17-31.
5. Aza-Blanc, P., F. Ramirez-Weber, M. Laget, C. Schwartz, and T. Kornberg. 1997. Proteolysis that is inhibited by Hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a represser. Cell 89: 1043-1053.
6. Basler, K. and G. Struhl. 1994. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368: 208-214.
7. Blackman, R.K., M. Sanicola, L.A. Raftery, T. Gillevet, and W.M. Gelbart. 1991. An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 111: 657-666.
8. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
9. Buscher, D., B. Bosse, J. Heymer, and U. Ruther. 1997. Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mech. Dev. 62: 175-182.
10. Capdevila, J. and I. Guerrero. 1994. Targeted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13: 4459-4468.
11. Chen, Y. and S. Struhl. 1996. Dual roles for patched in sequestering and transducing hedgehog. Cell 87: 553-563.
12. Chen, C.H., D.P. von Kessler, W. Park, B. Wang, Y. Ma, and P.A. Beachy. 1999. Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell 98: 305-316.
13. Chen, Y., N. Gallaher, R.H. Goodman, and S.M. Smolik. 1998. Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc. Natl. Acad. Sci. 95: 2349-2354.
14. Dai, P., H. Akimaru, T. Tanaka, T. Maekawa, M. Nakafuku, and S. Ishii. 1999. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274: 8143-8152.
15. Dean, M. 1996. Polarity, proliferation and the hedgehog pathway. Nat. Genet. 14: 245-247.
16. Ding, Q., J. Motoyama, S. Gasca, R. Mo, H. Sasaki, J. Rossant, and C.C. Hui. 1998. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125: 2533-2543.
17. Dominguez, M., M. Brunner, E. Hafen, and K. Basler. 1996. Sending and receiving the Hedgehog signal: Control by the Drosophila Gli protein Cubitus interruptus. Science 272: 1621-1625.
18. Goodrich, L.V. and M.P. Scott. 1998. Hedgehog and patched in neural development and disease. Neuron 21: 1243-1257.
19. Hammerschmidt, M., A. Brook, and A. McMahon. 1997. The world according to Hedgehog. Trends Genet. 13: 14-21.
20. Ingham, P.W. 1994. Hedgehog points the way. Curr. Biol. 4: 347-350.
21. _. 1998. Transducing Hedgehog: The story so far. EMBO J. 17: 3505-3511.
22. Jiang, J. and G. Struhl. 1995. Protein kinase A and Hedgehog signalling in Drosophila limb development. Cell 80: 563-572.
23. _. 1998. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391: 493-496.
24. Johnson, R.L., J.K. Grenier, and M.P. Scott. 1995. patched over-expression alters wing disc size and pattern: Transcriptional and post-transcriptional effects on hedgehog targets. Development 121: 4161-4170.
25. Krishnan, V., F.A. Pereira, Y. Qiu, C.H. Chen, P.A. Beachy, S.Y. Tsai, and M.J. Tsai. 1997. Mediation of Sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science 278: 1947-1950.
26. Lecuit, T., W.J. Brook, M. Ng, M. Callega, H. Sun, and S.M. Cohen. 1996. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381: 387-393.
27. Lee, J., K.A. Platt, P. Censullo, and A. Ruiz i Altaba. 1997. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124: 2537-2552.
28. Lepage, T., S.M. Cohen, F.J. Diaz-Benjumea, and S.M. Parkhurst. 1995. Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373: 711-715.
29. Li, W., J.T. Ohlmeyer, M.E. Lane, and D. Kalderon. 1995. Function of protein kinase A in hedghehog signal transduction and Drosophila imaginal disc development. Cell 80: 553-562.
30. Maniatis, T. 1999. A ubiquitin ligase complex essential for the NF-κB, Wnt/Wingless, and Hedgehog signaling pathways. Genes & Dev. 13: 505-510.
31. Matise, M.P., D.J. Epstein, H.L. Park, K.A. Platt, and A.L. Joyner. 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.
32. Methot, N. and K. Basler. 1999. Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell 96: 819-831.
33. Monnier, V., F. Dussillol, G. Alves, C. Lamour-Isnard, and A. Plessis. 1998. Suppressor of fused links fused and Cubitus interruptus on the hedgehog signalling pathway. Curr. Biol. 8: 583-586.
34. Motoyama, J., J. Liu, R. Mo, Q. Ding, M. Post, and C.C. Hui. 1998. Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat. Genet. 20: 54-57.
35. Motzny, C.K. and R. Holmgren. 1995. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 52: 137-150.
36. Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85: 357-368.
37. Ohlmeyer, J.T. and D. Kalderon. 1997. Dual pathways for induction of wingless expression by protein kinase A and Hedgehog in Drosophila embryos. Genes & Dev. 11: 2250-2258.
38. _. 1998. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396: 749-753.
39. Orenic, T.V., D.C. Slusarski, K.L. Kroll, and R.A. Holmgren. 1990. Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes & Dev. 4: 1053-1067.
40. Pan, D. and G.M. Rubin. 1995. cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80: 543-552.
41. Preat, T. 1992. Characterization of Suppressor of fused, a complete suppressor of the fused segment polarity gene of Drosophila melanogaster. Genetics 132: 725-736.
42. Robbins, D.J., K.E. Nybakken, R. Kobayashi, J.C. Sisson, J.M. Bishop, and P.P. Therond. 1997. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90: 225-234.
43. Ruiz i Altaba, A. 1997. Catching a Gli-mpse of Hedgehog. Cell 90: 193-196.
44. _. 1998. Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125: 2203-2212.
45. _. 1999. Gli proteins encode context-dependent positive and negative functions: Implications for development and disease. Development 126: 3205-3216.
46. Sisson, J.C., K.S. Ho, K. Suyama, and M.P. Scott. 1997. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90: 235-245.
47. Strigini, M. and S.M. Cohen. 1997. A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124: 4697-4705.
48. Struhl, G. and A. Adachi. 1998. Nuclear access and action of notch in vivo. Cell 93: 649-660.
49. Struhl, G. and K. Basler. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
50. Strutt, D.I., V. Wiersdorff, and M. Mlodzik. 1995. Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373: 705-709.
51. Tabata, T. and T.B. Kornberg. 1994. Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76: 89-102.
52. Theodosiou, N.A., S. Zhang, W.Y. Wang, and T. Xu. 1998. slimb coordinates wg and dpp expression in the dorsal-ventral and anterior-posterior axes during limb development. Development 125: 3411-3416.
53. Xu, T. and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
54. Zecca, M., K. Basler, and G. Struhl. 1995. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121: 2265-2278.