Altered localization of Drosophila smoothened protein activates hedgehog signal transduction

Genes and Development

Volumn 17, Issue 10, 2003, Pages 1240-1252

  Zhu, Alan Jian ^a   Zheng, Limin ^a   Suyama, Kaye ^a   Scott, Matthew P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Hedgehog; Patched; Smoothened

Indexed keywords

GREEN FLUORESCENT PROTEIN; KINESIN; MEMBRANE PROTEIN; MEMBRANE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; ENDOCYTOSIS; GENE; GENE ACTIVATION; GENETIC TRANSCRIPTION; INTERNALIZATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SALIVARY GLAND; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; MEMBRANE PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT FUSION PROTEINS; SALIVARY GLANDS; SIGNAL TRANSDUCTION;

ANIMALIA; ERINACEIDAE; HEXAPODA;

EID: 0038625111     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1080803     Document Type: Article

References (47)

1. Alcedo, J., Zou, Y., and Noll, M. 2000. Posttranscriptional regulation of smoothened is part of a self-correcting mechanism in the Hedgehog signaling system. Mol. Cell 6: 457-465.
2. Andrew, D.J., Henderson, K.D., and Seshaiah, P. 2000. Salivary gland development in Drosophila melanogaster. Mech. Dev. 92: 5-17.
3. Bailey, E.C., Scott, M.P., and Johnson, R.L. 2000. Hedgehog signaling in animal development and human disease. Ernst Schering Res. Found. Workshop 29: 211-235.
4. Benting, J.H., Rietveld, A.G., and Simons, K. 1999. N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J. Cell Biol. 146: 313-320.
5. Bucci, C., Parton, R.G., Mather, I.H., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. 1992. The small GTPase Rab5 functions as a regulator factor in the early endocytic pathway. Cell 70: 715-728.
6. Chen, J.K., Taipale, J., Cooper, M.K., and Beachy, P.A. 2002. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes & Dev. 16: 2743-2748.
7. Clark, I.E., Jan, L.Y., and Jan, Y.N. 1997. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124: 461-470.
8. DeCamp, D.L., Thompson, T.M., de Sauvage, F.J., and Lerner, M.R. 2000. Smoothened activates Gα-mediated signaling in frog melanophores. J. Biol. Chem. 275: 26322-26327.
9. Denef, N., Neubuser, D., Perez, L., and Cohen, S.M. 2000. Hedgehog induces opposite changes in turnover and subcellular localization of Patched and Smoothened. Cell 102: 521-531.
10. Eggenschwiler, J.T., Espinoza, E., and Anderson, K.V. 2001. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412: 194-198.
11. Entchev, E.V., Schwabedissen, A., and González-Gaitán, M. 2000. Gradient formation of the TGF-β homolog DPP. Cell 103: 981-991.
12. Forbes, A.J., Nakano, Y., Taylor, A.M., and Ingham, P.W. 1993. Genetic analysis of Hedgehog signalling in the Drosophila embryo. Dev. Suppl. 115-124.
13. Greco, V., Hannus, M., and Eaton, S. 2001. Argosomes: A potential vehicle for the spread of morphogens through epithelia. Cell 106: 633-645.
14. Hammerschmidt, M. and McMahon, A.P. 1998. The effect of pertussis toxin on zebrafish development: A possible role for inhibitory G-proteins in Hedgehog signaling. Dev. Biol. 194: 166-171.
15. Incardona, J.P., Gruenberg, J., and Roelink, H. 2002. Sonic hedgehog induces the segregation of Patched and Smoothened in endosomes. Curr. Biol. 12: 983-995.
16. Ingham, P.W. and Fietz, M.J. 1995. Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing. Curr. Biol. 5: 432-440.
17. Ingham, P.W. and McMahon, A.P. 2001. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15: 3059-3087.
18. Ingham, P.W., Nystedt, S., Nakano, Y., Brown, W., Stark, D., van den Heuvel, M., and Taylor, A.M. 2000. Patched represses the Hedgehog signalling pathway by promoting modification of the Smoothened protein. Curr. Biol. 10: 1315-1318.
19. Ioannou, Y.A. 2001. Multidrug permeases and subcellular cholesterol transport. Nat. Rev. Mol. Cell Biol. 2: 657-668.
20. Johnson, R.L., Grenier, J.K., and Scott, M.P. 1995. patched overexpression alters wing disc size and pattern: Transcriptional and post-transcriptional effects on hedgehog targets. Development 121: 4161-4170.
21. Johnson, R.L., Milenkovic, L., and Scott, M.P. 2000. In vivo functions of the Patched protein: Requirement of the C terminus for target gene inactivation but not Hedgehog sequestration. Mol. Cell 6: 467-478.
22. Kalderon, D. 2000. Transducing the hedgehog signal. Cell 103: 371-374.
23. Lee, J.J., Ekker, S.C., von Kessler, D.P., Porter, J.A., Sun, B.I., and Beachy, P.A. 1994. Autoproteolysis in hedgehog protein biogenesis. Science 266: 1528-1537.
24. Lotti, L.V., Mottola, G., Torrisi, M.R., and Bonatti, S. 1999. A different intracellular distribution of a single reporter protein is determined at steady state by KKXX or KDEL retrieval signals. J. Biol. Chem. 274: 10413-10420.
25. Lu, Z.L., Saldanha, J.W., and Hulme, E.C. 2002. Seven-transmembrane receptors: Crystals clarify. Trends Pharmacol. Sci. 23: 140-146.
26. McKay, R.R., Zhu, L., and Shortridge, R.D. 1995. A Drosophila gene that encodes a member of the protein disulfide isomerase/phospholipase-Cα family. Insect Biochem. Mol. Biol. 25: 647-654.
27. McLauchlan, H., Newell, J., Morrice, N., Osborne, A., West, M., and Smythe, E. 1998. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8: 34-45.
28. Martín, V., Carrillo, G., Torroja, C., and Guerrero, I. 2001. The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr. Biol. 11: 601-607.
29. Moline, M.M., Southern, C., and Bejsovec, A. 1999. Directionality of Wingless protein transport influences epidermal patterning in the Drosophila embryo. Development 126: 4375-4384.
30. Muñiz, M. and Riezman, H. 2000. Intracellular transport of GPI-anchored proteins. EMBO J. 19: 10-15
31. Munro, S. and Pelham, H.R. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899-907.
32. Nybakken, K. and Perrimon, N. 2002. Hedgehog signal transduction: Recent findings. Curr. Opin. Genet. Dev. 12: 503.
33. Porter, J.A., von Kessler, D.P., Ekker, S.C., Young, K.E., Lee, J.J., Moses, K., and Beachy, P.A. 1995. The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374: 363-366.
34. Quirk, J., van den Heuvel, M., Henrique, D., Marigo, V., Jones, T.A., Tabin, C., and Ingham, P.W. 1997. The smoothened gene and hedgehog signal transduction in Drosophila and vertebrate development. Cold Spring Harb. Symp. Quant. Biol. 62: 217-226.
35. Resh, M.D. 1999. Fatty acylation of proteins: New insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451: 1-16.
36. Robbins, D.J., Nybakken, K.E., Kobayashi, R., Sisson, J.C., Bishop, J.M., and Therond, P.P. 1997. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein Costal2. Cell 90: 225-234.
37. Sisson, J.C., Ho, K.S., Suyama, K., and Scott, M.P. 1997. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90: 235-245.
38. Somsel Rodman, J. and Wandinger-Ness, A. 2000. Rab GTPases coordinate endocytosis. J. Cell Sci. 113: 183-192.
39. Stegman, M.A., Vallance, J.E., Elangovan, G., Sosinski, J., Cheng, C., and Robbins, D.J. 2000. Identification of a tetrameric Hedgehog signaling complex. J. Biol. Chem. 275: 21809-21812.
40. Strittmatter, S.M., Igarashi, M., and Fishman, M.C. 1994. GAP43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J. Neurosci. 14: 5503-5513.
41. Strutt, H., Thomas, C., Nakano, Y., Stark, D., Neave, B., Taylor, A.M., and Ingham, P.W. 2001. Mutations in the sterol-sensing domain of Patched suggest a role for vesicular trafficking in Smoothened regulation. Curr. Biol. 11: 608-613.
42. Taipale, J., Chen, J.K., Cooper, M.K., Wang, B., Mann, R.K., Milenkovic, L., Scott, M.P., and Beachy, P.A. 2000. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406: 1005-1009.
43. Taipale, J., Cooper, M.K., Maiti, T., and Beachy, P.A. 2002. Patched acts catalytically to suppress the activity of Smoothened. Nature 418: 892-897.
44. van der Bliek, A.M., Redelmeier, T.E., Damke, H., Tisdale, E.J., Meyerowitz, E.M., and Schmid, S.L. 1993. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122: 553-563.
45. van Leeuwen, F., Samos, C.H., and Nusse, R. 1994. Biological activity of soluble Wingless protein in cultured Drosophila imaginal disc cells. Nature 368: 342-344.
46. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifulco, M., Bruni, C.B., and Bucci, C. 1997. Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272: 4391-4397.
47. Xie, J., Murone, M., Luoh, S.M., Ryan, A., Gu, Q., Zhang, C., Bonifas, J.M., Lam, C.W., Hynes, M., Goddard, A., et al. 1998. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391: 90-92.