Development, Vol 120, Issue 11 3275-3287, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis

IF Emery, V Bedian and GM Guild
Department of Biology, University of Pennsylvania, Philadelphia 19104-6018.

The steroid hormone ecdysone initiates metamorphosis in Drosophila melanogaster by activating a cascade of gene activity that includes primary response transcriptional regulators and secondary response structural genes. The Broad-Complex (BR-C) primary response gene is composed of several distinct genetic functions and encodes a family of related transcription factor isoforms. Our objective was to determine whether BR-C isoforms were components of the primary ecdysone response in all tissues and whether tissue-specific isoform expression is associated with tissue-specific metamorphic outcomes. We used specific antibody reagents that recognize and distinguish among the Z1, Z2 and Z3 BR-C protein isoforms to study protein expression patterns during the initial stages of metamorphosis. Western blot analyses demonstrated that BR-C isoforms are induced at the onset of metamorphosis, each with unique kinetics of induction and repression. Whole-mount immunostaining showed that the BR-C proteins accumulate in the nuclei of all larval and imaginal tissues indicating that the BR-C is induced as a primary response in many tissues. Several tissues express different levels and combinations of the BR-C isoforms suggesting that the BR-C is important in determining the tissue-specific outcome of many parallel ecdysone response cascades. For example, prepupal salivary glands (destined for histolysis during metamorphosis) express Z1 isoforms while imaginal discs (destined for cell differentiation and morphogenesis) shift from the synthesis of Z2 isoforms to the synthesis of Z1 isoforms. The prepupal central nervous system (destined for tissue remodeling) expresses all isoforms, with Z3 predominating. Salivary gland chromosome immunostaining indicated that BR-C proteins interact directly with numerous loci in the polytene genome. Finally, western blot analyses showed that distinct BR-C genetic functions can be correlated with single and specific BR-C protein isoforms.

This article has been cited by other articles:

				Y. Suzuki, J. W. Truman, and L. M. Riddiford The role of Broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa Development, February 1, 2008; 135(3): 569 - 577. [Abstract] [Full Text] [PDF]

				X. Zhou and L. M. Riddiford rosy Function Is Required for Juvenile Hormone Effects in Drosophila melanogaster Genetics, January 1, 2008; 178(1): 273 - 281. [Abstract] [Full Text] [PDF]

				M. R. Atkey, J.-F. B. Lachance, M. Walczak, T. Rebello, and L. A. Nilson Capicua regulates follicle cell fate in the Drosophila ovary through repression of mirror Development, June 1, 2006; 133(11): 2115 - 2123. [Abstract] [Full Text] [PDF]

				N. A. Siddall, E. A. McLaughlin, N. L. Marriner, and G. R. Hime The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity PNAS, May 30, 2006; 103(22): 8402 - 8407. [Abstract] [Full Text] [PDF]

				D. F. Erezyilmaz, L. M. Riddiford, and J. W. Truman The pupal specifier broad directs progressive morphogenesis in a direct-developing insect PNAS, May 2, 2006; 103(18): 6925 - 6930. [Abstract] [Full Text] [PDF]

				T. G. Wilson, Y. Yerushalmi, D. M. Donnell, and L. L. Restifo Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex Genetics, January 1, 2006; 172(1): 253 - 264. [Abstract] [Full Text] [PDF]

				J. Terashima and M. Bownes Translating Available Food Into the Number of Eggs Laid by Drosophila melanogaster Genetics, August 1, 2004; 167(4): 1711 - 1719. [Abstract] [Full Text] [PDF]

				X. Zhou, B. Zhou, J. W. Truman, and L. M. Riddiford Overexpression of broad: a new insight into its role in the Drosophila prothoracic gland cells J. Exp. Biol., March 1, 2004; 207(7): 1151 - 1161. [Abstract] [Full Text] [PDF]

				J. Z. Maines, L. M. Stevens, X. Tong, and D. Stein Drosophila dMyc is required for ovary cell growth and endoreplication Development, February 15, 2004; 131(4): 775 - 786. [Abstract] [Full Text] [PDF]

				D. J. Emlen and C. E. Allen Genotype to Phenotype: Physiological Control of Trait Size and Scaling in Insects Integr. Comp. Biol., November 1, 2003; 43(5): 617 - 634. [Abstract] [Full Text] [PDF]

				S. K. Pallavi and L. S. Shashidhara Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs Development, October 15, 2003; 130(20): 4931 - 4941. [Abstract] [Full Text] [PDF]

				A. Schwendemann and M. Lehmann Pipsqueak and GAGA factor act in concert as partners at homeotic and many other loci PNAS, October 1, 2002; 99(20): 12883 - 12888. [Abstract] [Full Text] [PDF]

				D. Cakouros, T. Daish, D. Martin, E. H. Baehrecke, and S. Kumar Ecdysone-induced expression of the caspase DRONC during hormone-dependent programmed cell death in Drosophila is regulated by Broad-Complex J. Cell Biol., June 10, 2002; 157(6): 985 - 996. [Abstract] [Full Text] [PDF]

				S. W. Kim, X. Fang, H. Ji, A. F. Paulson, J. M. Daniel, M. Ciesiolka, F. van Roy, and P. D. McCrea Isolation and Characterization of XKaiso, a Transcriptional Repressor That Associates with the Catenin Xp120ctn in Xenopus laevis J. Biol. Chem., March 1, 2002; 277(10): 8202 - 8208. [Abstract] [Full Text] [PDF]

				X. Zhou and L. M. Riddiford Broad specifies pupal development and mediates the 'status quo' action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca Development, January 5, 2002; 129(9): 2259 - 2269. [Abstract] [Full Text] [PDF]

				N. Renault, K. King-Jones, and M. Lehmann Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specific hormone response Development, October 1, 2001; 128(19): 3729 - 3737. [Abstract] [Full Text] [PDF]

				L. Dobens, E Martin-Blanco, A Martinez-Arias, F. Kafatos, and L. Raftery Drosophila puckered regulates Fos/Jun levels during follicle cell morphogenesis Development, January 5, 2001; 128(10): 1845 - 1856. [Abstract] [PDF]

				C. Brennan, T. Li, M Bender, F Hsiung, and K Moses Broad-complex, but not ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye Development, January 1, 2001; 128(1): 1 - 11. [Abstract] [PDF]

				J. Gates and C. S. Thummel An Enhancer Trap Screen for Ecdysone-Inducible Genes Required for Drosophila Adult Leg Morphogenesis Genetics, December 1, 2000; 156(4): 1765 - 1776. [Abstract] [Full Text]

				M. G. Carter, M. A. Johns, X. Zeng, L. Zhou, M. C. Zink, J. L. Mankowski, D. M. Donovan, and S. B. Baylin Mice deficient in the candidate tumor suppressor gene Hic1 exhibit developmental defects of structures affected in the Miller-Dieker syndrome Hum. Mol. Genet., February 12, 2000; 9(3): 413 - 419. [Abstract] [Full Text] [PDF]

				M Yamada, T Murata, S Hirose, G Lavorgna, E Suzuki, and H Ueda Temporally restricted expression of transcription factor betaFTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster Development, January 12, 2000; 127(23): 5083 - 5092. [Abstract] [PDF]

				T Li and M Bender A conditional rescue system reveals essential functions for the ecdysone receptor (EcR) gene during molting and metamorphosis in Drosophila Development, January 7, 2000; 127(13): 2897 - 2905. [Abstract] [PDF]

				M Schubiger and J. Truman The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids Development, January 3, 2000; 127(6): 1151 - 1159. [Abstract] [PDF]

				G. Tzolovsky, W.-M. Deng, T. Schlitt, and M. Bownes The Function of the Broad-Complex During Drosophila melanogaster Oogenesis Genetics, November 1, 1999; 153(3): 1371 - 1383. [Abstract] [Full Text]

				D. Sandstrom and L. Restifo Epidermal tendon cells require Broad Complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster J. Cell Sci., January 11, 1999; 112(22): 4051 - 4065. [Abstract] [PDF]

				M Buszczak, M. Freeman, J. Carlson, M Bender, L Cooley, and W. Segraves Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila Development, January 10, 1999; 126(20): 4581 - 4589. [Abstract] [PDF]

				H. Niu, B. H. Ye, and R. Dalla-Favera Antigen receptor signaling induces MAP kinase-mediated phosphorylation and degradation of the BCL-6 transcription factor Genes & Dev., July 1, 1998; 12(13): 1953 - 1961. [Abstract] [Full Text]

				C. Brennan, M Ashburner, and K Moses Ecdysone pathway is required for furrow progression in the developing Drosophila eye Development, January 7, 1998; 125(14): 2653 - 2664. [Abstract] [PDF]

				P. D'Avino and C. Thummel crooked legs encodes a family of zinc finger proteins required for leg morphogenesis and ecdysone-regulated gene expression during Drosophila metamorphosis Development, January 5, 1998; 125(9): 1733 - 1745. [Abstract] [PDF]

				J. C. Fletcher, P. P. D'Avino, and C. S. Thummel A steroid-triggered switch in E74 transcription factor isoforms regulates the timing of secondary-response gene expression PNAS, April 29, 1997; 94(9): 4582 - 4586. [Abstract] [Full Text] [PDF]

				W. Deng and M Bownes Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis Development, January 11, 1997; 124(22): 4639 - 4647. [Abstract] [PDF]

				C Jiang, E. Baehrecke, and C. Thummel Steroid regulated programmed cell death during Drosophila metamorphosis Development, January 11, 1997; 124(22): 4673 - 4683. [Abstract] [PDF]

				G. Lam, C Jiang, and C. Thummel Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis Development, January 5, 1997; 124(9): 1757 - 1769. [Abstract] [PDF]

				G Gonzy-Treboul, J A Lepesant, and J Deutsch Enhancer-trap targeting at the Broad-Complex locus of Drosophila melanogaster. Genes & Dev., May 1, 1995; 9(9): 1137 - 1148. [Abstract] [PDF]

				R. Hodgetts, W. Clark, S. O'Keefe, M Schouls, K Crossgrove, G. Guild, and L von Kalm Hormonal induction of Dopa decarboxylase in the epidermis of Drosophila is mediated by the Broad-Complex Development, January 11, 1995; 121(11): 3913 - 3922. [Abstract] [PDF]

				A. Andres and C. Thummel The Drosophila 63F early puff contains E63-1, an ecdysone-inducible gene that encodes a novel Ca(2+)-binding protein Development, January 8, 1995; 121(8): 2667 - 2679. [Abstract] [PDF]

				J. Fletcher and C. Thummel The Drosophila E74 gene is required for the proper stage- and tissue-specific transcription of ecdysone-regulated genes at the onset of metamorphosis Development, January 5, 1995; 121(5): 1411 - 1421. [Abstract] [PDF]

				J. Fletcher, K. Burtis, D. Hogness, and C. Thummel The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone Development, January 5, 1995; 121(5): 1455 - 1465. [Abstract] [PDF]

				N. Ghbeish, C.-C. Tsai, M. Schubiger, J. Y. Zhou, R. M. Evans, and M. McKeown The dual role of ultraspiracle, the Drosophila retinoid X receptor, in the ecdysone response PNAS, March 27, 2001; 98(7): 3867 - 3872. [Abstract] [Full Text] [PDF]