Vertebrate homologs of Drosophila Suppressor of fused interact with the Gli family of transcriptional regulators

Developmental Biology

Volumn 212, Issue 2, 1999, Pages 323-336

  Pearse II, Richard V ^a   Collier, Lara S ^b   Scott, Matthew P ^b   Tabin, Clifford J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENE PRODUCT; PROTEIN SERINE THREONINE KINASE;

ANIMAL TISSUE; ARTICLE; DNA BINDING; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALIA; AVES; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS; ERINACEIDAE; GALLUS GALLUS; MAMMALIA; MELANOGASTER; METAZOA; RODENTIA; VERTEBRATA;

EID: 0033566844     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9335     Document Type: Article

References (77)

1. Akiyama H., Shigeno C., Hiraki Y., Shukunami C., Kohno H., Akagi M., Konishi J., Nakamura T. Cloning of a mouse smoothened cDNA and expression patterns of hedgehog signalling molecules during chondrogenesis and cartilage differentiation in clonal mouse EC cells, ATDC5. Biochem. Biophys. Res. Commun. 235:1997;142-147.
2. 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.
3. 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.
4. 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.
5. Aruga J., Nagai T., Tokuyama T., Hayashizaki Y., Okazaki Y., Chapman V. M., Mikoshiba K. The mouse zic gene family. Homologues of the Drosophila pair-rule gene odd-paired. J. Biol. Chem. 271:1996a;1043-1047.
6. Aruga J., Yozu A., Hayashizaki Y., Okazaki Y., Chapman V. M., Mikoshiba K. Identification and characterization of Zic4, a new member of the mouse Zic gene family. Gene. 172:1996b;291-294.
7. Aruga J., Yokota N., Hashimoto M., Furuichi T., Fukuda M., Mikoshiba K. A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem. 63:1994;1880-1890.
8. 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.
9. Bitgood M. J., McMahon A. P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:1995;126-138.
10. Bitgood M. J., Shen L., McMahon A. P. Sertoli cell signaling by desert hedgehog regulates the male germline. Curr. Biol. 6:1996;298-304.
11. Breeden L., Nasmyth K. Regulation of the yeast HO gene. Cold Spring Harbor Symp. Quant. Biol. 50:1985;643-650.
12. Brewster R., Lee J., Ruiz i Altaba A. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature. 393:1998;579-583.
13. 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. Nat. Genet. 20:1998;180-183.
14. Buscher D., Bosse B., Heymer J., Ruther U. Evidence for genetic control of sonic hedgehog by Gli3 in mouse limb development. Mech. Dev. 62:1997;175-182.
15. 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.
16. Chidambaram A., Goldstein A. M., Gailani M. R., Gerrard B., Bale S. J., DiGiovanna J. J., Bale A. E., Dean M. Mutations in the human homologue of the Drosophila patched gene in Caucasian and African-American nevoid basal cell carcinoma syndrome patients. Cancer Res. 56:1996;4599-4601.
17. 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.
18. 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.
19. 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.
20. Fan H., Oro A. E., Scott M. P., Khavari P. A. Induction of basal cell carcinoma features in transgenic human skin expressing sonic hedgehog. Nat. Med. 3:1997;788-792.
21. Fietz M. J., Concordet J. P., Barbosa R., Johnson R., Krauss S., McMahon A. P., Tabin C., Ingham P. W. The hedgehog gene family in Drosophila and vertebrate development. Dev. Suppl. 1994;43-51.
22. Gietz D., St. Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1992;1425.
23. Goodrich L. V., Johnson R. L., Milenkovic L., McMahon J. A., Scott M. P. Conservation of the hedgehog/patched signaling pathway from flies to mice: Induction of a mouse patched gene by hedgehog. Genes Dev. 10:1996;301-312.
24. Goodrich L. V., Scott M. P. Hedgehog and patched in neural development and disease. Neuron. 21:1998;1243-1257.
25. Grindley J. C., Bellusci S., Perkins D., Hogan B. L. Evidence for the involvement of the Gli gene family in embryonic mouse lung development. Dev. Biol. 188:1997;337-348.
26. Hahn H., Wicking C., Zaphiropoulous P. G., Gailani M. R., Shanley S., Chidambaram A., Vorechovsky I., Holmberg E., Unden A. B., Gillies S., Negus K., Smyth I., Pressman C., Leffell D. J., Gerrard B., Goldstein A. M., Dean M., Toftgard R., Chenevix-Trench G., Wainwright B., Bale A. E. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell. 85:1996;841-851.
27. Hamburger V., Hamilton H. L. A series of normal stages in the development of the chick embryo. Dev. Dyn. 195:1992;231-272.
28. Hammerschmidt M., Brook A., McMahon A. P. The world according to hedgehog. Trends Genet. 13:1997;14-21.
29. Hidalgo A., Ingham P. Cell patterning in the Drosophila segment: Spatial regulation of the segment polarity gene patched. Development. 110:1990;291-301.
30. Hooper J. E., Scott M. P. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell. 59:1989;751-765.
31. Hughes D. C., Allen J., Morley G., Sutherland K., Ahmed W., Prosser J., Lettice L., Allan G., Mattei M. G., Farrall M., Hill R. E. Cloning and sequencing of the mouse Gli2 gene: Localization to the Dominant hemimelia critical region. Genomics. 39:1997;205-215.
32. Hui C. C., Joyner A. L. A mouse model of greig cephalopolysyndactyly syndrome: The extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3:1993;241-246.
33. Hui C. C., Slusarski D., Platt K. A., Holmgren R., Joyner A. L. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 162:1994;402-413.
34. Ingham P. W. Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature. 366:1993;560-562.
35. Ingham P. W. Transducing hedgehog: The story so far. EMBO J. 17:1998;3505-3511.
36. James P., Halladay J., Craig E. A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 144:1996;1425-1436.
37. Kinzler K. W., Bigner S. H., Bigner D. D., Trent J. M., Law M. L., S. J., O. B., Wong A. J., Vogelstein B. Identification of an amplified, highly expressed gene in a human glioma. Science. 236:1987;70-73.
38. 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.
39. 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.
40. Lee J. J., von Kessler D. P., Parks S., Beachy P. A. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell. 71:1992;33-50.
41. Marigo V., Davey R. A., Zuo Y., Cunningham J. M., Tabin C. J. Biochemical evidence that patched is the hedgehog receptor. Nature. 384:1996a;176-179.
42. Marigo V., Johnson R. L., Vortkamp A., Tabin C. J. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev. Biol. 180:1996b;273-283.
43. Marigo V., Tabin C. J. Regulation of patched by sonic hedgehog in the developing neural tube. Proc. Natl. Acad. Sci. USA. 93:1996;9346-9351.
44. 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.
45. 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.
46. Motoyama J., Takabatake T., Takeshima K., Hui C. Ptch2, a second mouse patched gene is co-expressed with sonic hedgehog. Nat. Genet. 18:1998;104-106.
47. Nagai T., Aruga J., Takada S., Gunther T., Sporle R., Schughart K., Mikoshiba K. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 182:1997;299-313.
48. 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.
49. Nakata K., Nagai T., Aruga J., Mikoshiba K. Xenopus zic family and its role in neural and neural crest development. Mech. Dev. 75:1998;43-51.
50. Nusslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 287:1980;795-801.
51. Ohlmeyer J. T., Kalderon D. Hedgehog stimulates maturation of cubitus interruptus into a labile transcriptional activator. Nature. 396:1998;749-753.
52. Orenic T. V., Slusarski D. C., Kroll K. L., Holmgren R. A. Cloning and characterization of the segment polarity gene cubitus interruptus dominant of Drosophila. Genes Dev. 4:1990;1053-1067.
53. 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.
54. 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.
55. Preat T. Characterization of suppressor of fused, a complete suppressor of the fused segment polarity gene of Drosophila melanogaster. Genetics. 132:1992;725-736.
56. 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.
57. 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.
58. Radhakrishna U., Wild A., Grzeschik K. H., Antonarakis S. E. Mutation in GLI3 in postaxial polydactyly type A. Nat. Genet. 17:1997;269-271.
59. Raffel C., Jenkins R. B., Frederick L., Hebrink D., Alderete B., Fults D. W., James C. D. Sporadic medulloblastomas contain PTCH mutations. Cancer Res. 57:1997;842-845.
60. Riddle R. D., Johnson R. L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75:1993;1401-1416.
61. Rimm D. L., Pollard T. D. New plasmid vectors for high level synthesis of eukaryotic fusion proteins in Escherichia coli. Gene. 75:1989;323-327.
62. 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.
63. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science. 234:1986;364-368.
64. Ruppert J. M., Vogelstein B., Arheden K., Kinzler K. W. GLI3 encodes a 190-kilodalton protein with multiple regions of GLI similarity. Mol. Cell. Biol. 10:1990;5408-5415.
65. Schreiber E., Matthias P., Muller M. M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17:1989;6419.
66. 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.
67. 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.
68. Tabata T., Kornberg T. B. Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell. 76:1994;89-102.
69. Taylor A. M., Nakano Y., Mohler J., Ingham P. W. Contrasting distributions of patched and hedgehog proteins in the Drosophila embryo. Mech. Dev. 42:1993;89-96.
70. 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.
71. Unden A. B., Holmberg E., Lundh-Rozell B., Stahle-Backdahl M., Zaphiropoulos P. G., Toftgard R., Vorechovsky I. Mutations in the human homologue of Drosophila patched (PTCH) in basal cell carcinomas and the Gorlin syndrome: Different in vivo mechanisms of PTCH inactivation. Cancer Res. 56:1996;4562-4565.
72. van den Heuvel M., Ingham P. W. Smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature. 382:1996;547-551.
73. Vorechovsky I., Unden A. B., Sandstedt B., Toftgard R., Stahle-Backdahl M. Trichoepitheliomas contain somatic mutations in the overexpressed PTCH gene: Support for a gatekeeper mechanism in skin tumorigenesis. Cancer Res. 57:1997;4677-4681.
74. Vortkamp A., Gessler M., Grzeschik K. H. GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature. 352:1991;539-540.
75. 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.
76. Wilkinson D. Whole mount in situ hybridization of vertebrate embryos. Wilkinson D. In Situ Hybridization: A Practical Approach. 1992;75-83 Oxford Univ. Press, New York.
77. 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.