Hedgehog signal transduction: From flies to vertebrates

Experimental Cell Research

Volumn 253, Issue 1, 1999, Pages 25-33

  Murone, Maximilien ^a   Rosenthal, Arnon ^a   De Sauvage, Frederic J ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN;

CARCINOGENESIS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONGENITAL MALFORMATION; DROSOPHILA MELANOGASTER; INVERTEBRATE; MORPHOGENESIS; MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

EID: 0033604515     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4676     Document Type: Article

References (104)

1. Hogan B. L. Morphogenesis. Cell. 96:1999;225-233.
2. Nusslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 287:1980;795-801.
3. Hammerschmidt M., Brook A., McMahon A. P. The world according to hedgehog. Trends Genet. 13:1997;14-21.
4. Echelard Y., Epstein D. J., St-Jacques B., Shen L., Mohler J., McMahon J. A., McMahon A. P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 75:1993;1417-1430.
5. Krauss S., Concordet J. P., Ingham P. W. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell. 75:1993;1431-1444.
6. Riddle R. D., Johnson R. L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75:1993;1401-1416.
7. Roelink H., Porter J. A., Chiang C., Tanabe Y., Chang D. T., Beachy P. A., Jessell T. M. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell. 81:1995;445-455.
8. Ericson J., Muhr J., Placzek M., Lints T., Jessell T. M., Edlund T. Sonic hedgehog induces the differentiation of ventral forebrain neurons: A common signal for ventral patterning within the neural tube. Cell. 81:1995;747-756.
9. Marti E., Bumcrot D. A., Takada R., McMahon A. P. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature. 375:1995;322-325.
10. Hynes M., Porter J. A., Chiang C., Chang D., Tessier-Lavigne M., Beachy P. A., Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron. 15:1995;35-44.
11. Laufer E., Nelson C. E., Johnson R. L., Morgan B. A., Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell. 79:1994;993-1003.
12. Schwabe J. W., Rodriguez-Esteban C., Izpisua Belmonte J. C. Limbs are moving: Where are they going. Trends Genet. 14:1998;229-235.
13. Fan C. M., Tessier-Lavigne M. Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog. Cell. 79:1994;1175-1186.
14. Johnson R. L., Laufer E., Riddle R. D., Tabin C. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell. 79:1994;1165-1173.
15. Roberts D. J., Johnson R. L., Burke A. C., Nelson C. E., Morgan B. A., Tabin C. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development. 121:1995;3163-3174.
16. Roberts D. J., Smith D. M., Goff D. J., Tabin C. J. Epithelial-mesenchymal signaling during the regionalization of the chick gut. Development. 125:1998;2791-2801.
17. Bellusci S., Furuta Y., Rush M., Henderson R., Winnier G., Hogan B. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Dev. Suppl. 124:1997;53-63.
18. Oro A. E., Higgins K. M., Hu Z., Bonifas J. M., Epstein E. H. Jr., Scott M. P. Basal cell carcinomas in mice overexpressing Sonic hedgehog. Science. 276:1997;817-821.
19. Oro A. E., Scott M. P. Splitting hairs: Dissecting roles of signaling systems in epidermal development. Cell. 95:1998;575-578.
20. Ramsdell A. F., Yost H. J. Molecular mechanisms of vertebrate left-right development. Trends Genet. 14:1998;459-465.
21. Chiang C., Litingtung Y., Lee E., Young K. E., Corden J. L., Westphal H., Beachy P. A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 383:1996;407-413.
22. Lanske B., Karaplis A. C., Lee K., Luz A., Vortkamp A., Pirro A., Karperien M., Defize L. H. K., Ho C., Mulligan R. C., Abou-Samra A. B., Juppner H., Segre G. V., Kronenberg H. M. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science. 273:1996;663-666.
23. Vortkamp A., Lee K., Lanske B., Segre G. V., Kronenberg H. M., Tabin C. J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 273:1996;613-622.
24. Bitgood M. J., Shen L., McMahon A. P. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr. Biol. 6:1996;298-304.
25. Perler F. B. Protein splicing of inteins and hedgehog autoproteolysis: Structure, function, and evolution. Cell. 92:1998;1-4.
26. Porter J. A., Young K. E., Beachy P. A. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274:1996;255-259.
27. Pepinsky R. B., Zeng C., Wen D., Rayhorn P., Baker D. P., Williams K. P., Bixler S. A., Ambrose C. M., Garber E. A., Miatkowski K., Taylor F. R., Wang E. A., Galdes A. Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273:1998;14037-14045.
28. Ericson J., Briscoe J., Rashbass P., van Heyningen V., Jessell T. M. Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb Symp. Quant. Biol. 62:1997;451-466.
29. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 394:1998;85-88.
30. McCormick C., Leduc Y., Martindale D., Mattison K., Esford L. E., Dyer A. P., Tufaro F. The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nature Genet. 19:1998;158-161.
31. Ramirez-Weber F. A., Kornberg T. B. Cytonemes: Cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell. 97:1999;599-607.
32. Nakano Y., Guerrero I., Hidalgo A., Taylor A., Whittle J. R., Ingham P. W. A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature. 341:1989;508-513.
33. Hooper J. E., Scott M. P. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell. 59:1989;751-765.
34. Alcedo J., Ayzenzon M., Von Ohlen T., Noll M., Hooper J. E. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell. 86:1996;221-232.
35. van den Heuvel M., Ingham P. W. Smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature. 382:1996;547-551.
36. Chen Y., Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 87:1996;553-563.
37. Johnson R. L., Scott M. P. Control of cell growth and fate by patched genes. Cold Spring Harb. Symp. Quant. Biol. 62:1997;205-215.
38. Goodrich L. V., Scott M. P. Hedgehog and patched in neural development and disease. Neuron. 21:1998;1243-1257.
39. Marigo V., Davey R. A., Zuo Y., Cunningham J. M., Tabin C. J. Biochemical evidence that patched is the Hedgehog receptor. Nature. 384:1996;176-179.
40. Stone D. M., Hynes M., Armanini M., Swanson T. A., Gu Q., Johnson R. L., Scott M. P., Pennica D., Goddard A., Phillips H., Noll M., Hooper J. E., de Sauvage F., Rosenthal A. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature. 384:1996;129-134.
41. Carpenter D., Stone D. M., Brush J., Ryan A., Armanini M., Frantz G., Rosenthal A., de Sauvage F. J. Characterization of two patched receptors for the vertebrate hedgehog protein family. Proc. Natl. Acad. Sci. USA. 95:1998;13630-13634.
42. Cooper M. K., Porter J. A., Young K. E., Beachy P. A. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science. 280:1998;1603-1607.
43. Incardona J. P., Gaffield W., Kapur R. P., Roelink H. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development. 125:1998;3553-3562.
44. Chen Y., Struhl G. In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex. Development. 125:1998;4943-4948.
45. Kinto N., Iwamoto M., Enomoto-Iwamoto M., Noji S., Ohuchi H., Yoshioka H., Kataoka H., Wada Y., Yuhao G., Takahashi H. E., Yoshiki S., Yamaguchi A. Fibroblasts expressing Sonic hedgehog induce osteoblast differentiation and ectopic bone formation. FEBS Lett. 404:1997;319-323.
46. Murone M., Rosenthal A., de Sauvage F. J. Sonic hedgehog signaling by the patched-smoothened receptor complex. Curr. Biol. 9:1999;76-84.
47. Quirk J., van den Heuvel M., Henrique D., Marigo V., Jones T. A., Tabin C., Ingham P. W. The smoothened gene and hedgehog signal transduction in Drosophila and vertebrate development. Cold Spring Harb. Symp. Quant. Biol. 62:1997;217-226.
48. Chuang P. T., McMahon A. P. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature. 397:1999;617-621.
49. Ingham P. W. Transducing Hedgehog: The story so far. EMBO J. 17:1998;3505-3511.
50. Kinzler K. W., Vogelstein B. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol. 10:1990;634-642.
51. Alexandre C., Jacinto A., Ingham P. W. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10:1996;2003-2013.
52. Von Ohlen T., Lessing D., Nusse R., Hooper J. E. Hedgehog signaling regulates transcription through cubitus interruptus, a sequence-specific DNA binding protein. Proc. Natl. Acad. Sci. USA. 94:1997;2404-2409.
53. Sasaki H., Hui C., Nakafuku M., Kondoh H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development. 124:1997;1313-1322.
54. Aza-Blanc P., Ramirez-Weber F. A., Laget M. P., Schwartz C., Kornberg T. B. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell. 89:1997;1043-1053.
55. Chen Y., Gallaher N., Goodman R. H., Smolik S. M. Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc. Natl. Acad. Sci. USA. 95:1998;2349-2354.
56. Chen Y., Cardinaux J. R., Goodman R. H., Smolik S. M. Mutants of cubitus interruptus that are independent of PKA regulation are independent of hedgehog signaling. Development. 126:1999;3607-3616.
57. Jiang J., Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature. 391:1998;493-496.
58. Chen C.-H., von Kesseler D. P., Park W., Wang P., Ma Y., Beachy P. A. Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of hedgehog target gene expression. Cell. 98:1999;305-316.
59. Ohlmeyer J. T., Kalderon D. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature. 396:1998;749-753.
60. Methot N., Basler K. Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell. 96:1999;819-831.
61. Preat T., Therond P., Lamour-Isnard C., Limbourg-Bouchon B., Tricoire H., Erk I., Mariol M. C., Busson D. A putative serine/threonine protein kinase encoded by the segment-polarity fused gene of Drosophila. Nature. 347:1990;87-89.
62. Therond P., Alves G., Limbourg-Bouchon B., Tricoire H., Guillemet E., Brissard-Zahraoui J., Lamour-Isnard C., Busson D. Functional domains of fused, a serine-threonine kinase required for signaling in Drosophila. Genetics. 142:1996;1181-1198.
63. Therond P. P., Knight J. D., Kornberg T. B., Bishop J. M. Phosphorylation of the fused protein kinase in response to signaling from hedgehog. Proc. Natl. Acad. Sci. USA. 93:1996;4224-4228.
64. Preat T. Characterization of Suppressor of fused, a complete suppressor of the fused segment polarity gene of Drosophila melanogaster. Genetics. 132:1992;725-736.
65. Pham A., Therond P., Alves G., Tournier F. B., Busson D., Lamour-Isnard C., Bouchon B. L., Preat T., Tricoire H. The Suppressor of fused gene encodes a novel PEST protein involved in Drosophila segment polarity establishment. Genetics. 140:1995;587-598.
66. Alves G., Limbourg-Bouchon B., Tricoire H., Brissard-Zahraoui J., Lamour-Isnard C., Busson D. Modulation of Hedgehog target gene expression by the Fused serine-threonine kinase in wing imaginal discs. Mech. Dev. 78:1998;17-31.
67. Robbins D. J., Nybakken K. E., Kobayashi R., Sisson J. C., Bishop J. M., Therond P. P. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell. 90:1997;225-234.
68. Preat T., Therond P., Limbourg-Bouchon B., Pham A., Tricoire H., Busson D., Lamour-Isnard C. Segmental polarity in Drosophila melanogaster: Genetic dissection of fused in a Suppressor of fused background reveals interaction with costal-2. Genetics. 135:1993;1047-1062.
69. Rechsteiner M., Rogers S. W. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:1996;267-271.
70. Akimaru H., Chen Y., Dai P., Hou D. X., Nonaka M., Smolik S. M., Armstrong S., Goodman R. H., Ishii S. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature. 386:1997;735-738.
71. Ohlmeyer J. T., Kalderon D. Dual pathways for induction of wingless expression by protein kinase A and Hedgehog in Drosophila embryos. Genes Dev. 11:1997;2250-2258.
72. Zhong H., SuYang H., Erdjument-Bromage H., Tempst P., Ghosh S. The transcriptional activity of NF-kappaB is regulated by the IkappaB- associated PKAc subunit through a cyclic AMP-independent mechanism. Cell. 89:1997;413-424.
73. Sisson J. C., Ho K. S., Suyama K., Scott M. P. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell. 90:1997;235-245.
74. Monnier V., Dussillol F., Alves G., Lamour-Isnard C., Plessis A. Suppressor of fused links fused and Cubitus interruptus on the hedgehog signalling pathway. Curr. Biol. 8:1998;583-586.
75. Krishnan V., Pereira F. A., Qiu Y., Chen C. H., Beachy P. A., Tsai S. Y., Tsai M. J. Mediation of Sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science. 278:1997;1947-1950.
76. Sontag E., Nunbhakdi-Craig V., Bloom G. S., Mumby M. C. A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128:1995;1131-1144.
77. Hammerschmidt M., Bitgood M. J., McMahon A. P. Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev. 10:1996;647-658.
78. Pearse R. V. 2nd, Collier L. S., Scott M. P., Tabin C. J. Vertebrate homologs of Drosophila suppressor of fused interact with the Gli family of transcriptional regulators. Dev. Biol. 212:1999;323-336.
79. Marigo V., Johnson R. L., Vortkamp A., Tabin C. J. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev. Biol. 180:1996;273-283.
80. Lee J., Platt K. A., Censullo P., Ruiz i Altaba A. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development. 124:1997;2537-2552.
81. Hynes M., Stone D. M., Dowd M., Pitts-Meek S., Goddard A., Gurney A., Rosenthal A. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron. 19:1997;15-26.
82. Ruiz i Altaba A. Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development. 125:1998;2203-2212.
83. Theil T., Kaesler S., Grotewold L., Bose J., Ruther U. Gli genes and limb development. Cell Tissue Res. 296:1999;75-83.
84. Liu F., Massague J., Ruiz i Altaba A. Carboxy-terminally truncated Gli3 proteins associate with Smads. Nature Genet. 20:1998;325-326.
85. Matise M. P., Epstein D. J., Park H. L., Platt K. A., Joyner A. L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development. 125:1998;2759-2770.
86. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C. C. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development. 125:1998;2533-2543.
87. Mo R., Freer A. M., Zinyk D. L., Crackower M. A., Michaud J., Heng H. H., Chik K. W., Shi X. M., Tsui L. C., Cheng S. H., Joyner A. L., Hui C. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development. 124:1997;113-123.
88. Motoyama J., Liu J., Mo R., Ding Q., Post M., Hui C. C. Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nature Genet. 20:1998;54-57.
89. Dai P., Akimaru H., Tanaka Y., Maekawa T., Nakafuku M., Ishii S. Sonic hedgehog-induced activation of the gli1 promoter is mediated by GLI3. J. Biol. Chem. 274:1999;8143-8152.
90. Ruiz-i-Altaba A. Gli proteins encode context-dependent positive and negative functions: Implications for development and disease. Development. 126:1999;3205-3216.
91. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: Implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development. 126:1999;3915-3924.
92. Graves L. E., Segal S., Goodwin E. B. TRA-1 regulates the cellular distribution of the tra-2 mRNA in C. elegans. Nature. 399:1999;802-805.
93. Lewis K. E., Drossopoulou G., Paton I. R., Morrice D. R., Robertson K. E., Burt D. W., Ingham P. W., Tickle C. Expression of ptc and gli genes in talpid3 suggests bifurcation in Shh pathway. Development. 126:1999;2397-2407.
94. Belloni E., Muenke M., Roessler E., Traverso G., Siegel-Bartelt J., Frumkin A., Mitchell H. F., Donis-Keller H., Helms C., Hing A. V., Heng H. H., Koop B., Martindale D., Rommens J. M., Tsui L. C., Scherer S. W. Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nature Genet. 14:1996;353-356.
95. Ingham P. W. The patched gene in development and cancer. Curr. Opin. Genet. Dev. 8:1998;88-94.
96. Goodrich L. V., Milenkovic L., Higgins K. M., Scott M. P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science. 277:1997;1109-1113.
97. Hahn H., Wojnowski L., Zimmer A. M., Hall J., Miller G., Zimmer A. Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nature Med. 4:1998;619-622.
98. Xie J., Murone M., Luoh S. M., Ryan A., Gu Q., Zhang C., Bonifas J. M., Lam C. W., Hynes M., Goddard A., Rosenthal A., Epstein E. H. Jr., de Sauvage F. J. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature. 391:1998;90-92.
99. Reifenberger J., Wolter M., Weber R. G., Megahed M., Ruzicka T., Lichter P., Reifenberger G. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res. 58:1998;1798-1803.
100. Kinzler K. W., Bigner S. H., Bigner D. D., Trent J. M., Law M. L., O'Brien S. J., Wong A. J., Vogelstein B. Identification of an amplified, highly expressed gene in a human glioma. Science. 236:1987;70-73.
101. Dahmane N., Lee J., Robins P., Heller P., Ruiz i Altaba A. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature. 389:1997;876-881.
102. Ruppert J. M., Vogelstein B., Kinzler K. W. The zinc finger protein GLI transforms primary cells in cooperation with adenovirus E1A. Mol. Cell. Biol. 11:1991;1724-1728.
103. Shin S. H., Kogerman P., Lindstrom E., Toftgard R., Biesecker L. G. GLI3 mutations in human disorders mimic Drosophila cubitus interruptus protein functions and localization. Proc. Natl. Acad. Sci. USA. 96:1999;2880-2884.
104. Brown S. A., Warburton D., Brown L. Y., Yu C. Y., Roeder E. R., Stengel-Rutkowski S., Hennekam R. C., Muenke M. Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nature Genet. 20:1998;180-183.