Genetic Screens to Identify Elements of the decapentaplegic Signaling Pathway in Drosophila

INVESTIGATIONS

Genetic Screens to Identify Elements of the decapentaplegic Signaling Pathway in Drosophila

L. A. Raftery, V. Twombly, K. Wharton and W. M. Gelbart
Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts 02129, and Department of Cell and Developmental Biology, Harvard University, Cambridge, Massachusetts 02138

Pathways for regulation of signaling by transforming growth factor-{beta} family members are poorly understood at present. The best genetically characterized member of this family is encoded by the Drosophila gene decapentaplegic (dpp), which is required for multiple events during fly development. We describe here the results of screens for genes required to maximize dpp signaling during embryonic dorsal-ventral patterning. Screens for genetic interactions in the zygote have identified an allele of tolloid, as well as two novel alleles of screw, a gene recently shown to encode another bone morphogenetic protein-like polypeptide. Both genes are required for patterning the dorsalmost tissues of the embryo. Screens for dpp interactions with maternally expressed genes have identified loss of function mutations in Mothers against dpp and Medea. These mutations are homozygous pupal lethal, engendering gut defects and severely reduced imaginal disks, reminiscent of dpp mutant phenotypes arising during other dpp-dependent developmental events. Genetic interaction phenotypes are consistent with reduction of dpp activity in the early embryo and in the imaginal disks. We propose that the novel screw mutations identified here titrate out some component(s) of the dpp signaling pathway. We propose that Mad and Medea encode rate-limiting components integral to dpp pathways throughout development.

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				M. C. Wilkes, H. Mitchell, S. G. Penheiter, J. J. Dore, K. Suzuki, M. Edens, D. K. Sharma, R. E. Pagano, and E. B. Leof Transforming Growth Factor-{beta} Activation of Phosphatidylinositol 3-Kinase Is Independent of Smad2 and Smad3 and Regulates Fibroblast Responses via p21-Activated Kinase-2 Cancer Res., November 15, 2005; 65(22): 10431 - 10440. [Abstract] [Full Text] [PDF]

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				Y. Chai, Y. Ito, and J. Han TGF-{beta} SIGNALINGANDITS FUNCTIONAL SIGNIFICANCEIN REGULATINGTHE FATEOF CRANIAL NEURAL CREST CELLS Crit. Rev. Oral. Biol. Med., March 1, 2003; 14(2): 78 - 88. [Abstract] [Full Text]

				Z. A. Quinn, C.-C. Yang, J. L. Wrana, and J. C. McDermott Smad proteins function as co-modulators for MEF2 transcriptional regulatory proteins Nucleic Acids Res., February 1, 2001; 29(3): 732 - 742. [Abstract] [Full Text] [PDF]

				M. A. Su, R. G. Wisotzkey, and S. J. Newfeld A Screen for Modifiers of decapentaplegic Mutant Phenotypes Identifies lilliputian, the Only Member of the Fragile-X/Burkitt's Lymphoma Family of Transcription Factors in Drosophila melanogaster Genetics, February 1, 2001; 157(2): 717 - 725. [Abstract] [Full Text]

				M. R. DiChiara, J. M. Kiely, M. A. Gimbrone , Jr., M.-E. Lee, M. A. Perrella, and J. N. Topper Inhibition of E-Selectin Gene Expression by Transforming Growth Factor {beta} in Endothelial Cells Involves Coactivator Integration of Smad and Nuclear Factor {kappa}B-mediated Signals J. Exp. Med., September 5, 2000; 192(5): 695 - 704. [Abstract] [Full Text] [PDF]

				R. T. Cox, D. G. McEwen, D. L. Myster, R. J. Duronio, J. Loureiro, and M. Peifer A Screen for Mutations That Suppress the Phenotype of Drosophila armadillo, the {beta}-Catenin Homolog Genetics, August 1, 2000; 155(4): 1725 - 1740. [Abstract] [Full Text]

				K. Kitamura, S.-i. Aota, R. Sakamoto, S.-I. Yoshikawa, and K. Okazaki Smad7 selectively interferes with different pathways of activin signaling and inhibits erythroid leukemia cell differentiation Blood, June 1, 2000; 95(11): 3371 - 3379. [Abstract] [Full Text] [PDF]

				R. Fernandez, F. Takahashi, Z. Liu, R. Steward, D. Stein, and E. R. Stanley The Drosophila Shark tyrosine kinase is required for embryonic dorsal closure Genes & Dev., March 1, 2000; 14(5): 604 - 614. [Abstract] [Full Text]

				K Kubota, S Goto, K Eto, and S Hayashi EGF receptor attenuates Dpp signaling and helps to distinguish the wing and leg cell fates in Drosophila Development, January 9, 2000; 127(17): 3769 - 3776. [Abstract] [PDF]

				F Peri and S Roth Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg Development, January 2, 2000; 127(4): 841 - 850. [Abstract] [PDF]

				E. PIEK, C.-H. HELDIN, and P. TEN DIJKE Specificity, diversity, and regulation in TGF-{beta} superfamily signaling FASEB J, December 1, 1999; 13(15): 2105 - 2124. [Abstract] [Full Text]

				H.-J. Zhu, J. Iaria, and A. M. Sizeland Smad7 Differentially Regulates Transforming Growth Factor beta -mediated Signaling Pathways J. Biol. Chem., November 5, 1999; 274(45): 32258 - 32264. [Abstract] [Full Text] [PDF]

				Y. Sun, X. Liu, E. Ng-Eaton, H. F. Lodish, and R. A. Weinberg SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor beta signaling PNAS, October 26, 1999; 96(22): 12442 - 12447. [Abstract] [Full Text] [PDF]

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				R Hays, K. Buchanan, C Neff, and T. Orenic Patterning of Drosophila leg sensory organs through combinatorial signaling by hedgehog, decapentaplegic and wingless Development, January 7, 1999; 126(13): 2891 - 2899. [Abstract] [PDF]

				M Hild, A Dick, G. Rauch, A Meier, T Bouwmeester, P Haffter, and M Hammerschmidt The smad5 mutation somitabun blocks Bmp2b signaling during early dorsoventral patterning of the zebrafish embryo Development, January 5, 1999; 126(10): 2149 - 2159. [Abstract] [PDF]

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				J. Thatcher, C Haun, and P. Okkema The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx Development, January 1, 1999; 126(1): 97 - 107. [Abstract] [PDF]

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				P. E. Mead, Y. Zhou, K. D. Lustig, T. L. Huber, M. W. Kirschner, and L. I. Zon Cloning of Mix-related homeodomain proteins using fast retrieval of gel shift activities, (FROGS), a technique for the isolation of DNA-binding proteins PNAS, September 15, 1998; 95(19): 11251 - 11256. [Abstract] [Full Text] [PDF]