Transduction of the Hedgehog signal through the dimerization of Fused and the nuclear translocation of Cubitus interruptus

Cell Research

Volumn 21, Issue 10, 2011, Pages 1436-1451

  Zhang, Yanyan ^a   Mao, Feifei ^a   Lu, Yi ^a   Wu, Wenqing ^a   Zhang, Lei ^a   Zhao, Yun ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

Cubitus interruptus; Drosophila; Fused; Hedgehog; morphogen

Indexed keywords

CI PROTEIN, DROSOPHILA; COS PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; FUSED PROTEIN, DROSOPHILA; G PROTEIN COUPLED RECEPTOR; HEDGEHOG PROTEIN, DROSOPHILA; KINESIN; PROTEIN SERINE THREONINE KINASE; SMOOTHENED PROTEIN, DROSOPHILA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR;

ACTIVE TRANSPORT; ANIMAL; ARTICLE; CELL LINE; CELL NUCLEUS; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE; CELL NUCLEUS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEDGEHOG PROTEINS; KINESIN; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

CUBITUS INTERRUPTUS; ERINACEIDAE; INVERTEBRATA; METAZOA; VERTEBRATA;

EID: 80053647419     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2011.136     Document Type: Article

References (47)

1. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001;15:3059-3087. (Pubitemid 33115673)
2. Taipale J, Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001;411:349-354. (Pubitemid 32467044)
3. Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev Cell 2008;15:801-812.
4. Pospisilik JA, Schramek D, Schnidar H, et al. Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 2010;140:148-160.
5. Varjosalo M, Taipale J. Hedgehog: functions and mechanisms. Genes Dev 2008;22:2454-2472.
6. Alcedo J, Ayzenzon M, Von Ohlen T, Noll M, Hooper JE. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 1996;86:221-232. (Pubitemid 26286105)
7. Aikin RA, Ayers KL, Therond PP. The role of kinases in the Hedgehog signalling pathway. EMBO Rep 2008;9:330-336.
8. Zhang C, Williams EH, Guo Y, Lum L, Beachy PA. Extensive phosphorylation of Smoothened in Hedgehog pathway activation. Proc Natl Acad Sci USA 2004;101:17900-17907. (Pubitemid 40054047)
9. Jia J, Tong C, Wang B, Luo L, Jiang J. Hedgehog signalling activity of Smoothened requires phosphorylation by protein kinase A and casein kinase I. Nature 2004;432:1045-1050. (Pubitemid 40052237)
10. Apionishev S, Katanayeva NM, Marks SA, Kalderon D, Tomlinson A. Drosophila Smoothened phosphorylation sites essential for Hedgehog signal transduction. Nat Cell Biol 2005;7:86-92. (Pubitemid 40123387)
11. Jia J, Tong C, Jiang J. Smoothened transduces Hedgehog signal by physically interacting with Costal2/Fused complex through its C-terminal tail. Genes Dev 2003;17:2709-2720. (Pubitemid 37363075)
12. Ruel L, Rodriguez R, Gallet A, Lavenant-Staccini L, Therond PP. Stability and association of Smoothened, Costal2 and Fused with Cubitus interruptus are regulated by Hedgehog. Nat Cell Biol 2003;5:907-913. (Pubitemid 37220697)
13. Lum L, Zhang C, Oh S, et al. Hedgehog signal transduction via Smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2. Mol Cell 2003;12:1261-1274. (Pubitemid 37487933)
14. Ogden SK, Ascano M Jr, Stegman MA, et al. Identification of a functional interaction between the transmembrane protein Smoothened and the kinesin-related protein Costal2. Curr Biol 2003;13:1998-2003. (Pubitemid 37425211)
15. Liu Y, Cao X, Jiang J, Jia J. Fused-Costal2 protein complex regulates Hedgehog-induced Smo phosphorylation and cellsurface accumulation. Genes Dev 2007;21:1949-1963. (Pubitemid 47204933)
16. Ascano M Jr, Robbins DJ. An intramolecular association between two domains of the protein kinase Fused is necessary for Hedgehog signaling. Mol Cell Biol 2004;24:10397-10405. (Pubitemid 39507876)
17. Zhao Y, Tong C, Jiang J. Hedgehog regulates smoothened activity by inducing a conformational switch. Nature 2007;450:252-258. (Pubitemid 350100532)
18. Piston DW, Kremers GJ. Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem Sci 2007;32:407-414. (Pubitemid 47369164)
19. Malpel S, Claret S, Sanial M, et al. The last 59 amino acids of Smoothened cytoplasmic tail directly bind the protein kinase Fused and negatively regulate the Hedgehog pathway. Dev Biol 2007;303:121-133. (Pubitemid 46241093)
20. Robbins DJ, Nybakken KE, Kobayashi R, et al. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 1997;90:225-234. (Pubitemid 27329708)
21. Sisson JC, Ho KS, Suyama K, Scott MP. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 1997;90:235-245. (Pubitemid 27329709)
22. Zhang W, Zhao Y, Tong C, et al. Hedgehog-regulated Costal2-kinase complexes control phosphorylation and proteolytic processing of Cubitus interruptus. Dev Cell 2005;8:267-278. (Pubitemid 40197742)
23. Farzan SF, Ascano M Jr, Ogden SK, et al. Costal2 functions as a kinesin-like protein in the hedgehog signal transduction pathway. Curr Biol 2008;18:1215-1220.
24. Gazdoiu S, Yamoah K, Wu K, et al. Proximity-induced activation of human Cdc34 through heterologous dimerization. Proc Natl Acad Sci USA 2005;102:15053-15058. (Pubitemid 41513333)
25. Clackson T, Yang W, Rozamus LW, et al. Redesigning an FKBP-ligand interface to generate chemical dimerizers with novel specificity. Pro Natl Acad Sci USA 1998;95:10437-10442. (Pubitemid 28413085)
26. Rigden MD, Baier C, Ramirez-Arcos S, et al. Identification of the coiled-coil domains of Enterococcus faecalis DivIVA that mediate oligomerization and their importance for biological function. J Biochem 2008;144:63-76. (Pubitemid 351958443)
27. Raisin S, Ruel L, Ranieri N, Staccini-Lavenant L, Therond PP. Dynamic phosphorylation of the kinesin Costal-2 in vivo reveals requirement of fused kinase activity for all levels of hedgehog signalling. Dev Biol 2010;344:119-128.
28. Nybakken KE, Turck CW, Robbins DJ, Bishop JM. Hedgehog-stimulated phosphorylation of the kinesin-related protein Costal2 is mediated by the serine/threonine kinase fused. J Biol Chem 2002;277:24638-24647. (Pubitemid 34951993)
29. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000;103:211-225.
30. Chen CH, von Kessler DP, Park W, et al. Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell 1999;98:305-316. (Pubitemid 29380566)
31. Humke EW, Dorn KV, Milenkovic L, Scott MP, Rohatgi R. The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. Genes Dev 2010;24:670-682.
32. Wang QT, Holmgren RA. Nuclear import of cubitus interruptus is regulated by hedgehog via a mechanism distinct from Ci stabilization and Ci activation. Development 2000;127:3131-3139. (Pubitemid 30611905)
33. Wang QT, Holmgren RA. The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development 1999;126:5097-5106. (Pubitemid 30000422)
34. Wang G, Amanai K, Wang B, Jiang J. Interactions with Costal2 and suppressor of fused regulate nuclear translocation and activity of cubitus interruptus. Genes Dev 2000;14:2893-2905.
35. Seong KH, Akimaru H, Dai P, et al. Inhibition of the nuclear import of cubitus interruptus by roadkill in the presence of strong hedgehog signal. PloS One 2010;5:e15365.
36. Briscoe J, Sussel L, Serup P, et al. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 1999;398:622-627. (Pubitemid 29183690)
37. Hooper JE, Scott MP. Communicating with Hedgehogs. Nat Rev 2005;6:306-317. (Pubitemid 40516897)
38. Lecuit T, Brook WJ, Ng M, et al. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 1996;381:387-393. (Pubitemid 26164704)
39. Nellen D, Burke R, Struhl G, Basler K. Direct and long-range action of a DPP morphogen gradient. Cell 1996;85:357-368. (Pubitemid 26160707)
40. Strigini M, Cohen SM. Formation of morphogen gradients in the Drosophila wing. Sem Cell Dev Biol 1999;10:335-344. (Pubitemid 129502428)
41. Zhao Y, Tong C, Jiang J. Transducing the Hedgehog signal across the plasma membrane. Fly 2007;1:333-336.
42. Xia L, Jia S, Huang S, et al. The Fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response. Cell 2010;143:978-990.
43. Narbonne-Reveau K, Besse F, Lamour-Isnard C, Busson D, Pret AM. fused regulates germline cyst mitosis and differentiation during Drosophila oogenesis. Mech Dev 2006;123:197-209.
44. Claret S, Sanial M, Plessis A. Evidence for a novel feedback loop in the Hedgehog pathway involving Smoothened and Fused. Curr Biol 2007;17:1326-1333. (Pubitemid 47189707)
45. Motzny CK, Holmgren R. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech Dev 1995;52:137-150.
46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 2001;25:402-408. (Pubitemid 34164012)
47. Gesellchen V, Kuttenkeuler D, Steckel M, Pelte N, Boutros M. An RNA interference screen identifies Inhibitor of Apoptosis Protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep 2005;6:979-984. (Pubitemid 41521955)