A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A

Development

Volumn 125, Issue 9, 1998, Pages 1759-1768

  Chen, Yijing ^a   Riese, Matthew J ^a   Killinger, Mark A ^a   Hoffmann, F Michael ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

60A; dpp; Drosophila; Mad; Modifier screen; punt; TGF

Indexed keywords

POLYPEPTIDE; TRANSFORMING GROWTH FACTOR BETA;

ALLELE; ANIMAL TISSUE; ARTICLE; DEVELOPMENTAL GENETICS; DIFFERENTIATION; DNA SEQUENCE; DROSOPHILA; ECTODERM; EMBRYO; ENHANCER REGION; FAT BODY; IMAGINAL DISC; MESODERM; MIDGUT; MORPHOGENESIS; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VISCERA;

ACTIVIN RECEPTORS; ANIMALS; BONE MORPHOGENETIC PROTEINS; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENETIC COMPLEMENTATION TEST; INSECT PROTEINS; MESODERM; MUTATION; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, GROWTH FACTOR; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; ARACHNIDA; HEXAPODA;

EID: 0031860761     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Affolter, M., Nellen, D., Nussbaumer, U. and Basler, K. (1994). Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF-β homologs during Drosophila embryogenesis. Development 120, 3105-3117.
2. Aono, A., Hazama, M., Notoya, K., Taketomi, S., Yamasaki, H., Tsukuda, R., Sasaki, S. and Fujisawa, Y. (1995). Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210, 670-677.
3. Arora, K., Dai, H., Kazuko, S. G., Jamal, J., O'Connor, M. B., Letsou, A. and Warrior, R. (1995). The Drosophila schnurri gene acts in the Dpp/TGF-β signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81, 781-790.
4. Arora, K., Levine, M. S. and O'Connor, M. B. (1994). The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev. 8, 2588-2601.
5. Ashburner, M. (1989). Drosophila: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
6. Bienz, M. (1994). Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet. 10, 22-26.
7. Brook, W. J., Diaz-Benjumea, F. J. and Cohen, M. S. (1996). Organizing spatial pattern in limb development. Annu. Rev. Cell Dev. Biol. 12, 161-180.
8. Brummel, T. J., Twombly, V., Marqué, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massagué, J., O'Connor, M. B. and Gelbart, W. M. (1994). Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78, 251-261.
9. Burke, R. and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Dmsophila wing. Development 122, 2261-2269.
10. Capovilla, M., Brandt, M. and Botas, J. (1994). Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Cell 76, 461-475.
11. Childs, S. R., Wrana, J. L., Arora, K., Attisano, L., O'Connor, M. B. and Massagué, J. (1993). Identification of a Drosophila activin receptor. Proc. Natl Acad. Sci. USA 90, 9475-9479.
12. Derynck, R. and Zhang, Y. (1996). Intracellular signalling: the mad way to do it. Curr. Biol. 6, 1226-1229.
13. Doctor, J. S., Jackson, P. D., Rashka, K. E., Visalli, M. and Hoffmann, F. M. (1992). Sequence, biochemical characterization, and developmental expression of a new member of the TGF-β superfamily in Drosophila melanogaster. Dev. Biol. 151, 491-505.
14. Eppert, K., Scherer, S. W., Ozcelik, H., Pirone, R., Hoodless, P., Kim, H., Tsui, L. C., Bapat, B., Gallinger, S., Andrulis, I. L., Thomsen, G. H., Wrana, J. L. and Attisano, L. (1996). MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543-552.
15. Ferguson, E. L. and Anderson, K. V. (1992a). decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
16. Ferguson, E. L. and Anderson, K. V. (1992b). Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
17. Gertler, F. B., Doctor, J. S. and Hoffmann, F. M. (1990). Genetic suppression of mutations in the Drosophila abl Proto-oncogene homolog. Science 248, 857-860.
18. Grieder, N. C., Nellen, D., Burke, R., Basler, K. and Affolter, M. (1995). schnurri is required for Drosophila dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 81, 791-800.
19. Hata, A., Lo, R. S., Wotton, D., Lagna, G. and Massagué, J. (1997). Mutations increasing autoinhibition inactivate tumour suppressors Samd2 and Smad4. Nature 388, 82-87.
20. Hazama, M., Aono, A., Ueno, N. and Fujisawa, Y. (1995). Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system. Biochem. Biophys. Res. Commun. 209, 859-866.
21. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
22. Hou, X.S., Goldstein, E.S. and Perrimon, N. (1997). Drosophiia Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev. 11, 1728-1737.
23. Hursh, D. A., Padgett, R. W. and Gelbart, W. M. (1993). Cross regulation of decapentaplegic and Ultrabithorax transcription in the embryonic visceral mesoderm of Drosophila. Development 117, 1211-1222.
24. Immerglück, K., Lawrence, P. A. and Bienz, M. (1990). Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62, 261-268.
25. Jackson, P. D. and Hoffmann, F. M. (1994). Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression. Developmental Dynamics 199, 28-44.
26. Kim, J., Johnson, K., Chen, H. J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
27. Kingsley, D. M. (1994a). The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 133-146.
28. Kingsley, D. M. (1994b). What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet. 10, 16-21.
29. Letsou, A., Arora, K., Wrana, J. L., Simin, K., Twombly, V., Jamal, J., Staehling-Hampton, K., Hoffmann, F. M., Gelbart, W. M., Massagué, J. and et al. (1995). Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGFβ receptor family. Cell 80, 899-908.
30. Lyons, K. M., Hogan, B. L. and Robertson, E. J. (1995). Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50, 71-83.
31. Massagué, J. (1996). TGF-β signaling: receptors, transducers, and Mad proteins. Cell 85, 947-950.
32. Massagué, J., Attisano, L. and Wrana, J. L. (1994). The TGF-β family and its composite receptors. Trends Cell Biol. 4, 172-178.
33. Massagué, J. and Weis-Garcia, F. (1996). Serine/threonine kinase receptors: mediators of transforming growth factor β family signals. Cancer Surv. 27, 41-64.
34. Masucci, J. D. and Hoffmann, F. M. (1993). Identification of two regions from the Drosophila decapentaplegic gene required for embryonic midgut development and larval viability. Dev. Biol. 159, 276-287.
35. Masucci, J. D., Miltenberger, R. J. and Hoffmann, F. M. (1990). Pattern- specific expression of the Drosophila decopentaplegic gene in imaginal disks is regulated by 3′ cis-regulatory elements. Genes Dev. 4, 2011-2023.
36. Miyazono, K., Ichijo, H. and C-H., H. (1993). Transforming growth factor- β latent forms, binding proteins and receptors. Growth Factors 8, 11-22.
37. Nellen, D., Affolter, M. and Basler, K. (1994). Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78, 225-237.
38. Newfeld, S. J., Chartoff, E. H., Graff, J. M., Melton, D. A. and Gelbart, W. M. (1996). Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development 122, 2099- 2108.
39. Newfeld, S. J., Mehra, A., Singer, M. A., Wrana, J. L., Attisano, L. and Gelbart, W. M. (1997). Mothers against dpp participates in a DPP/TGF-β responsive serine-threonine kinase signal transduction cascade. Development 124, 3167-3176.
40. Padgett, R. W., St. Johnston, R. D. and Gelbart, W. M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 81-84.
41. Padgett, R. W., Wozney, J. M. and Gelbart, W. M. (1993). Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 90, 2905-2909.
42. Panganiban, G. E. F., Rashka, K. E., Neitzel, M. D. and Hoffmann, F. M. (1990a). Biochemical characterization of the Drosophila Dpp protein, a member of the transforming growth factor-β family of growth factors. Mol. Cell. Biol. 10, 2669-2677.
43. Panganiban, G. E. F., Reuter, R., Scott, M. P. and Hoffmann, F. M. (1990b). A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110, 1041-1050.
44. Penton, A., Chen, Y., Staehling-Hampton, K., Wrana, J. L., Attisano, L., Szidonya, J., Cassill, J. A., Massagué, J. and Hoffmann, F. M. (1994). Identification of two bone rnorphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 78, 239-250.
45. Raftery, L. A., Twombly, V., Wharton, K. and Gelbart, W. M. (1995). Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241-254.
46. Riesgo-Escovar, J.R. and Hafen, E. (1997). Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP- 1 transcription factor DJun during dorsal closure. Genes Dev. 11, 1717- 1727.
47. Reuter, R., Panganiban, G. E. F., Hoffmann, F. M. and Scott, M. P. (1990). Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110, 1031-1040.
48. Reuter, R. and Scott, M. P. (1990). Expression and function of the homeotic genes Antennapedia and Sex combs reduced in the embryonic midgut of Drosophila. Development 109, 289-303.
49. Roberts, A. B. and Sporn, M. B. (1990). The transforming growth factor- betas. In Peptide growth factors and their receptors, (ed. M. B. Sporn and A. B. Roberts), pp. 419-472. Springer-Verlag, Heidelberg
50. Ruberte, E., Narty, T., Nellen, D., Affolter, M. and Basler, K. (1995). An absolute requirement for both the type II and type I receptors. Punt and thickveins, for dpp signaling in vivo. Cell 80, 889-897.
51. Sampath, T. K., Rashka, K. E., Doctor, J. S., Tucker, R. F. and Hoffmann, F. M. (1993). Drosophila TGF-β superfamily proteins induce endochondral bone formation in mammals. Proc. Natl. Acad. Sci USA 90, 6004-6008.
52. Sekelsky, J., Newfeld, S. J., Raftery, L. A., Chartoff, E. H. and Gelbart, W. M. (1995). Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-1358.
53. Shi, Y., Hata, A., Lo, R. S., Massagué, J. and Pavletich, N. P. (1997). A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature 388, 87-93.
54. Simon, M. A., Bowtell, D. D. L., Dodson, G. S., Laverty, T. R. and Rubin, G. M. (1991). Ras 1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the Sevenless protein tyrosine kinase. Cell 67, 701-716.
55. Singer, M. A., Penton, A., Twombly, V., Hoffmann, F. M. and Gelbart, W. M. (1997). Signaling through both type I DPP receptors is required for anterior-posterior patterning of the entire Drosophila wing. Development 124, 79-89.
56. Spencer, F. A., Hoffmann, F. M. and Gelbart, W. M. (1982). Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28, 451-461.
57. St. Johnston, R. D. and Gelbart, W. D. (1987). Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 6, 2785-2791.
58. Staehling-Hampton, K. and Hoffmann, F. M. (1994). Ectopic decapentaplegic in the Drosophila midgut alters the express-ion of five homeotic genes, dpp and wingless, causing morphological defects. Dev. Biol 164, 502-512.
59. Staehling-Hampton, K., Hoffmann, F. M., Baylies, M. K., Rushton, E. and Bate, M. (1994). dpp induces mesodermal gene expression in Drosophila. Nature 372, 783-786.
60. Staehling-Hampton, K., Laughon, A. S. and Hoffmann, F. M. (1995). A Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development 121, 3393-3403.
61. Struhl, G. (1989). Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338, 741-744.
62. Sun, B., Hursh, D. A., Jackson, D. and Beachy, P. A. (1995). Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J. 14, 520-535.
63. Suzuki, A., Kaneko, E., Maeda, J. and Ueno, N. (1997). Mesoderm induction by BMP-4 and -7 heterodimers. Biochem. Biophys. Res. Commun. 232, 153-156.
64. Thüringer, F., Cohen, S. M. and Bienz, M. (1993a). Dissection of an indirect autoregulatory response of a homeotic Drosophila gene. EMBO J. 12, 2419- 2430.
65. Thüringer, F., Cohen, S. M. and Bienz, M. (1993b). Indirect autoregulation of a homeotic Drosophila gene mediated by extracellular signaling. Proc. Natl. Acad. Sci. USA 90, 3899-3903.
66. Tremml, G. and Bienz, M. (1989). Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J. 8, 2677-2685.
67. Twombly, V., Blackman, R. K., Jin, H., Graff, J. M., Padgett, R. W. and Gelbart, W. M. (1996). The TGF-β signaling pathway is essential for Drosophila oogenesis. Development 122, 1555-1565.
68. Wharton, K. A., Ray, R. P. and Gelbart, W. M. (1993). An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822.
69. Wharton, K. A., Thomsen, G. H. and Gelbart, W. M. (1991). Drosophila 60A gene, a new TGF-β family member is closely related to human bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 88, 9214-9218.
70. Wrana, J. L. and Pawson, T. (1997). Mad about SMADs. Nature 388, 28-29.
71. Xie, T., Finelli, A. L. and Padgett, R. W. (1994). The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGF-β superfamily. Science 263, 1756-1759.