A genetic screen in Drosophila for identifying novel components of the Hedgehog signaling pathway

Genetics

Volumn 170, Issue 1, 2005, Pages 173-184

  Collins, Russell T ^a,b   Cohen, Stephen M ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EIF1A PROTEIN; ERF1 PROTEIN; KINESIN; KINESIN LIKE PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLELISM; ANIMAL TISSUE; ARTICLE; CANCER; CARCINOGENESIS; CLINICAL PATHWAY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENE ISOLATION; GENE LOCUS; GENE MUTATION; GENETIC SCREENING; GENOTYPE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EUKARYOTIC INITIATION FACTOR-1; EYE PROTEINS; HOMEODOMAIN PROTEINS; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE TERMINATION FACTORS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; ERINACEIDAE; METAZOA;

EID: 20444431256     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.039420     Document Type: Article

References (78)

1. ABDELILAH-SEYFRIED, S., Y. M. CHAN, C. ZENG, N. J. JUSTICE, S. YOUNGER-SHEPHERD et al., 2001 A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 157: 455-456.
2. ADAMS, R. R., A. A. TAVARES, A. SALZBERG, H. J. BELLEN and D. M. GLOVER, 1998 pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12: 1483-1494.
3. 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: 221-232.
4. ALCEDO, J., Y. ZOU and M. NOLL, 2000 Posttranscriptional regulation of smoothened is part of a self-correcting mechanism in the Hedgehog signaling system. Mol. Cell 6: 457-465.
5. AZA-BLANC, P., F. A. RAMIREZ-WEBER, M. P. LAGET, C. SCHWARTZ and T. B. KORNBERG, 1997 Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89: 1043-1053.
6. HERMAN, D. M., S. S. KARHADKAR, A. MAITRA, R. MONTES DE OCA, M. R. GERSTENBLITH et al., 2003 Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 425: 846-851.
7. BRIZUELA, B. J., L. ELFRING, J. BALLARD, J. W. TAMKUN and J. A. KENNISON, 1994 Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics 137: 803-813.
8. BROOK, W. J., 2000 Hedgehog signaling and the axial patterning of Drosophila wings. Biochem. Cell Biol. 78: 585-591.
9. BUMCROT, D. A., R. TAKADA and A. P. MCMAHON, 1995 Proteolytic processing yields two secreted forms of sonic hedgehog. Mol. Cell. Biol. 15: 2294-2303.
10. BURKE, R., D. NELLEN, M. BELLOTTO, E. HAFEN, K. A. SENTI et al., 1999 Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 99: 803-815.
11. CAPDEVILA, J., M. P. ESTRADA, E. SANCHEZ-HERRERO and I. GUERRERO, 1994 The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 13: 71-82.
12. CHAMOUN, Z., R. K. MANN, D. NELLEN, D. P. VON KESSLER, M. BELLOTTO et al., 2001 Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 293: 2080-2084.
13. CHEN, B., T. CHU, E. HARMS, J. P. GERGEN and S. STRICKLAND, 1998 Mapping of Drosophila mutations using site-specific male recombination. Genetics 149: 157-163.
14. CHEN, Y., and G. STRUHL, 1996 Dual roles for patched in sequestering and transducing Hedgehog. Cell 87: 553-563.
15. 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. USA 95: 2349-2354.
16. CROZATIER, M., B. GLISE and A. VINCENT, 2002 Connecting Hh, Dpp and EGF signalling in patterning of the Drosophila wing: the pivotal role of collier/knot in the AP organiser. Development 129: 4261-4269.
17. DENEF, N., D. NEUBUSER, L. PEREZ and S. M., COHEN, 2000 Hedgehog induces opposite changes in turnover and subcellular localization of patched and smoothened. Cell 102: 521-531.
18. DESAI, C. J., J. G. GINDHART, JR., L. S. GOLDSTEIN and K. ZINN, 1996 Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84: 599-609.
19. ENTCHEV, E. V., A. SCHWABEDISSEN and M. GONZALEZ-GAITAN, 2000 Gradient formation of the TGF-beta homolog Dpp. Cell 103: 981-991.
20. FLYBASE, 2003 The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 31: 172-175.
21. GARBE, J. C., E. YANG and J. W. FRISTROM, 1993 IMP-L2: an essential secreted immunoglobulin family member implicated in neural and ectodermal development in Drosophila. Development 119: 1237-1250.
22. GOMEZ-SKARMETA, J. L., and J. MODOLELL, 1996 araucan and caupolican provide a link between compartment subdivisions and patterning of sensory organs and veins in the Drosophila wing. Genes Dev. 10: 2935-2945.
23. HAN, C., T. Y. BELENKAYA, M. KHODOUN, M. TAUCHI and X. LIN, 2004 Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development 131: 1563-1575.
24. HARRISON, D. A., and N. PERRIMON, 1993 Simple and efficient generation of marked clones in Drosophila. Curr. Biol. 3: 424-433.
25. HOOPER, J. E., 1994 Distinct pathways for autocrine and paracrine Wingless signalling in Drosophila embryos. Nature 372: 461-464.
26. INGHAM, P. W., and A. P. MCMAHON, 2001 Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15: 3059-3087.
27. JIA, J., K. AMANAI, G. WANG, J. TANG, B. WANG et al., 2002 Shaggy/ GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature 416: 548-552.
28. JIA, J., C. TONG and J. JIANG, 2003 Smoothened transduces Hedgehog signal by physically interacting with Costal2/Fused complex through its C-terminal tail. Genes Dev. 17: 2709-2720.
29. JIANG, J., and G. STRUHL, 1998 Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391: 493-496.
30. KEHL, B. T., K. O. CHO and K. W. CHOI, 1998 mirror, a Drosophila homeobox gene in the Iroquois complex, is required for sensory organ and alula formation. Development 125: 1217-1227.
31. KISSELEV, L. L., and R. H. BUCKINGHAM, 2000 Translational termination comes of age. Trends Biochem. Sci. 25: 561-566.
32. LAMBERTSSON, A., 1998 The minute genes in Drosophila and their molecular functions. Adv. Genet. 38: 69-134.
33. LASKO, P., 2000 The Drosophila melanogaster genome: translation factors and RNA binding proteins. J. Cell Biol. 150: F51-F56.
34. LECUIT, T., W. J. BROOK, M. NG, M. CALLEJA, H. SUN et al., 1996 Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381: 387-393.
35. LEE, J. D., and J. E. TREISMAN, 2001 Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr. Biol. 11: 1147-1152.
36. LEE, J. J., S. C. EKKER, D. P. VON KESSLER, J. A. PORTER, B. I. SUN et al., 1994 Autoproteolysis in hedgehog protein biogenesis. Science 266: 1528-1537.
37. LUM, L., C. ZHANG, S. OH, R. K. MANN, D. P. VON KESSLER et al., 2003 Hedgehog signal transduction via Smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2. Mol. Cell 12: 1261-1274.
38. MARTI, E., and P. BOVOLENTA, 2002 Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci. 25: 89-96.
39. MCNEILL, H., C. H. YANG, M. BRODSKY, J. UNGOS and M. A. SIMON, 1997 mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev. 11: 1073-1082.
40. 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.
41. METHOT, N., and K. BASLER, 2000 Suppressor of fused opposes hedgehog signal transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus. Development 127: 4001-4010.
42. MICCHELLI, C. A., I. THE, E. SELVA, V. MOGILA and N. PERRIMON, 2002 Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 129: 843-851.
43. MINESTRINI, G., A. S. HARLEY and D. M. GLOVER, 2003 Localization of Pavarotti-KLP in living Drosophila embryos suggests roles in reorganizing the cortical cytoskeleton during the mitotic cycle. Mol. Biol. Cell 14: 4028-4038.
44. 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.
45. MULLOR, J. L., M. CALLEJA, J. CAPDEVILA and I. GUERRERO, 1997 Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning. Development 124: 1227-1237.
46. MYRICK, K. V., and C. R. DEAROLF, 2000 Hyperactivation of the Drosophila Hopjak kinase causes the preferential overexpression of eIF1A transcripts in larval blood cells. Gene 244: 119-125.
47. NELLEN, D., R. BURKE, G. STRUHL and K. BASLER, 1996 Direct and long-range action of a DPP morphogen gradient. Cell 85: 357-368.
48. NEUMANN, C. J., and S. M. COHEN, 1997 Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124: 871-880.
49. OGDEN, S. K., M. ASCANO, JR., M. A. STEGMAN, L. M. SUBER, J. E. HOOPER et al., 2003 Identification of a functional interaction between the transmembrane protein Smoothened and the kinesin-related protein Costal2. Curr. Biol 13: 1998-2003.
50. OU, C. Y., Y. F. LIN, Y. J. CHEN and C. T. CHIEN, 2002 Distinct protein degradation mechanisms mediated by Cul1 and Cul3 controlling Ci stability in Drosophila eye development. Genes Dev. 16: 2403-2414.
51. PENA-RANGEL, M. T., I. RODRIGUEZ and J. R. RIESGO-ESCOVAR, 2002 A misexpression study examining dorsal thorax formation in Drosophila melanogaster. Genetics 160: 1035-1050.
52. PERSSON, U., H. IZUMI, S. SOUCHELNYTSKVI, S. ITOH, S. GRIMSBY et al., 1998 The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434: 83-87.
53. PESTOVA, T. V., V. G. KOLUPAEVA, I. B. LOMAKIN, E. V. PILIPENKO, I. N. SHATSKY et al., 2001 Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98: 7029-7036.
54. PORTER, J. A., D. P. VON KESSLER, S. C. EKKER, K. E. YOUNG, J. J. LEE et al., 1995 The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374: 363-366.
55. PRICE, M. A., and D. KAEDERON, 1999 Proteolysis of cubitus interruptus in Drosophila requires phosphorylation by protein kinase A. Development 126: 4331-4339.
56. PRICE, M. A., and D. KALDERON, 2002 Proteolysis of the Hedgehog signaling effector Cubitus interruptus requires phosphorylation by glycogen synthase kinase 3 and casein kinase 1. Cell 108: 823-835.
57. QUIRK, J., M. VAN DEN HEUVEL, D. HENRIQUE, V. MARIGO, T. A. JONES et al., 1997 The smoothened gene and hedgehog signal transduction in Drosophila and vertebrate development. Cold Spring Harbor Symp. Quant. Biol. 62: 217-226.
58. ROBBINS, D. J., K. E. NYBAKKEN, R. KOBAYASHI, J. C. SISSON, J. M. BISHOP et al., 1997 Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90: 225-234.
59. RUEl, L., R. RODRIGUEZ, A. GALLET, L. LAVENANT-STACCINI and P. P. THEROND, 2003 Stability and association of Smoothened, Costal2 and Fused with Cubitus interruptus are regulated by Hedgehog. Nat. Cell Biol. 5: 907-913.
60. RUIZ I ALTABA A., P. SANCHEZ and N. DAHMANE, 2002 Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2: 361-372.
61. RYDER, E., F. BEOWS, M. ASHBURNER, R. BAUTISTA-LLACER, D. COULSON et al., 2004 The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167: 797-813.
62. 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.
63. STRIGINI, M., and S. M. COHEN, 1997 A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124: 4697-4705.
64. STRIGINI, M., and S. M. COHEN, 2000 Wingless gradient formation in the Drosophila wing. Curr. Biol. 10: 293-300.
65. TABATA, T., and Y. TAKEI, 2004 Morphogens, their identification and regulation. Development 131: 703-712.
66. TAIPALE, J., M. K. COOPER, T. MAITI and P. A. BEACHY, 2002 Patched acts catalytically to suppress the activity of Smoothened. Nature 418: 892-897.
67. TAKEI, Y., Y. OZAWA, M. SATO, A. WATANABE and T. TABATA, 2004 Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 131: 73-82.
68. TELKMAN, A. A., and S. M. COHEN, 2000 Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103: 971-980.
69. THAYER, S. P., M. P. DI MAGLIANO, P. W. HEISER, C. M. NIELSEN, D. J. ROBERTS et al., 2003 Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 425: 851-856.
70. THE, I., Y. BELLAICHE and N. PERRIMON, 1999 Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell 4: 633-639.
71. 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.
72. VAN DEN HEUVEL, M., and P. W. INGHAM, 1996 smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382: 547-551.
73. WANG, G., K. AMANAI, B. WANG and J. JIANG, 2000 Interactions with Costal2 and suppressor of fused regulate nuclear translocation and activity of cubitus interruptus. Genes Dev. 14: 2893-2905.
74. WATKINS, D. N., D. M. HERMAN, S. G. BURKHOLDER, B. WANG, P. A. BEACHY et al., 2003 Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 422: 313-317.
75. WU, J., and S. M. COHEN, 1999 Proximodistal axis formation in the Drosophila leg: subdivision into proximal and distal domains by Homothorax and Distal-less. Development 126: 109-117.
76. ZECCA, M., K. BASLER and G. STRUHL, 1996 Direct and long-range action of a wingless morphogen gradient. Cell 87: 833-844.
77. ZHAI, R. G., P. R. HIESINGER, T. W. KOH, P. VERSTREKEN, K. L. SCHULZE et al., 2003 Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA 100: 10860-10865.
78. ZHU, A. J., L. ZHENG, K. SUYAMA and M. P. SCOTT, 2003 Altered localization of Drosophila Smoothened protein activates Hedgehog signal transduction. Genes Dev. 17: 1240-1252.