The Ecdysone and Notch Pathways Synergistically Regulate Cut at the Dorsal–Ventral Boundary in Drosophila Wing Discs

Dongyu Jia; Jamal Bryant; Allison Jevitt; Gabriel Calvin; Wu-Min Deng

doi:10.1016/j.jgg.2016.03.002

Volume 43 Issue 4

Apr. 2016

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Article Navigation > Journal of Genetics and Genomics > 2016 > 43(4): 179-186

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The Ecdysone and Notch Pathways Synergistically Regulate Cut at the Dorsal–Ventral Boundary in Drosophila Wing Discs

doi: 10.1016/j.jgg.2016.03.002

Department of Biological Science, Florida State University, Tallahassee, FL 32306-4295, USA

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Corresponding author: E-mail address: wumin@bio.fsu.edu (Wu-Min Deng)
Received Date: 2015-11-30
Accepted Date: 2016-03-04
Rev Recd Date: 2016-02-05

Available Online: 2016-03-17

Publish Date: 2016-04-20

Abstract

Abstract

Metazoan development requires coordination of signaling pathways to regulate patterns of gene expression. In Drosophila, the wing imaginal disc provides an excellent model for the study of how signaling pathways interact to regulate pattern formation. The determination of the dorsal–ventral (DV) boundary of the wing disc depends on the Notch pathway, which is activated along the DV boundary and induces the expression of the homeobox transcription factor, Cut. Here, we show that Broad (Br), a zinc-finger transcription factor, is also involved in regulating Cut expression in the DV boundary region. However, Br expression is not regulated by Notch signaling in wing discs, while ecdysone signaling is the upstream signal that induces Br for Cut upregulation. Also, we find that the ecdysone-Br cascade upregulates cut-lacZ expression, a reporter containing a 2.7 kb cut enhancer region, implying that ecdysone signaling, similar to Notch, regulates cut at the transcriptional level. Collectively, our findings reveal that the Notch and ecdysone signaling pathways synergistically regulate Cut expression for proper DV boundary formation in the wing disc. Additionally, we showbr promotes Delta, a Notch ligand, near the DV boundary to suppress aberrant high Notch activity, indicating further interaction between the two pathways for DV patterning of the wing disc.
- Ecdysone,
- Notch,
- Broad,
- Cut,
- Wing disc,
- Dorsal–ventral boundary

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References(42)

References

[1]	Andersson, E.R., Sandberg, R., Lendahl, U. Notch signaling: simplicity in design, versatility in function Development, 138 (2011),pp. 3593-3612
[2]	Brown, H.L., Cherbas, L., Cherbas, P. et al. Development, 133 (2006),pp. 275-285
[3]	Buszczak, M., Freeman, M.R., Carlson, J.R. et al. Development, 126 (1999),pp. 4581-4589
[4]	Cherbas, L., Hu, X., Zhimulev, I. et al. Development, 130 (2003),pp. 271-284
[5]	de Celis, J.F., Bray, S. Development, 124 (1997),pp. 3241-3251
[6]	de Celis, J.F., Garcia-Bellido, A. Mech. Dev., 46 (1994),pp. 109-122
[7]	de Celis, J.F., Garcia-Bellido, A., Bray, S.J. Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc Development, 122 (1996),pp. 359-369
[8]	DiBello, P.R., Withers, D.A., Bayer, C.A. et al. Genetics, 129 (1991),pp. 385-397
[9]	Emery, I.F., Bedian, V., Guild, G.M. Development, 120 (1994),pp. 3275-3287
[10]	Fletcher, J.C., Thummel, C.S. Genetics, 141 (1995),pp. 1025-1035
[11]	Fortini, M.E. Notch signaling: the core pathway and its posttranslational regulation Dev. Cell, 16 (2009),pp. 633-647
[12]	Golic, K.G., Lindquist, S. Cell, 59 (1989),pp. 499-509
[13]	Gonzalez, A., Chaouiya, C., Thieffry, D. Genetics, 174 (2006),pp. 1625-1634
[14]	Guruharsha, K.G., Kankel, M.W., Artavanis-Tsakonas, S. The Notch signalling system: recent insights into the complexity of a conserved pathway Nat. Rev. Genet., 13 (2012),pp. 654-666
[15]	Heck, B.W., Zhang, B., Tong, X. et al. Biol. Open, 1 (2012),pp. 182-196
[16]	Hu, X., Cherbas, L., Cherbas, P. Transcription activation by the ecdysone receptor (EcR/USP): identification of activation functions Mol. Endocrinol., 17 (2003),pp. 716-731
[17]	Huppert, S.S., Jacobsen, T.L., Muskavitch, M.A. Development, 124 (1997),pp. 3283-3291
[18]	Ishimoto, H., Kitamoto, T. Fly (Austin), 5 (2011),pp. 215-220
[19]	Jack, J., Dorsett, D., Delotto, Y. et al. Development, 113 (1991),pp. 735-747
[20]	Jia, D., Huang, Y.C., Deng, W.M. Methods Mol. Biol., 1328 (2015),pp. 207-216
[21]	Jia, D., Tamori, Y., Pyrowolakis, G. et al. Dev. Biol., 392 (2014),pp. 52-61
[22]	Karim, F.D., Guild, G.M., Thummel, C.S. Development, 118 (1993),pp. 977-988
[23]	Klusza, S., Deng, W.M. Bioessays, 33 (2011),pp. 124-134
[24]	Lipikorn, R., Chunhapongpipat, K., Sirisup, S. et al. Medical image segmentation using modified level-set model with multi-scale gradient* vector flow Commun. Comput. Inf. Sci., 123 (2010),pp. 49-57
[25]	Mirth, C.K., Truman, J.W., Riddiford, L.M. Development, 136 (2009),pp. 2345-2353
[26]	Mullor, J.L., Calleja, M., Capdevila, J. et al. Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning Development, 124 (1997),pp. 1227-1237
[27]	Neumann, C.J., Cohen, S.M. Development, 122 (1996),pp. 3477-3485
[28]	Nijhout, H.F., Callier, V. Developmental mechanisms of body size and wing-body scaling in insects Annu. Rev. Entomol., 60 (2015),pp. 141-156
[29]	Palmer, W.H., Jia, D., Deng, W.M. eLife, 3 (2014),p. e04415
[30]	Pignoni, F., Zipursky, S.L. Development, 124 (1997),pp. 271-278
[31]	Restrepo, S., Zartman, J.J., Basler, K. Coordination of patterning and growth by the morphogen DPP Curr. Biol., 24 (2014),pp. R245-R255
[32]	Saj, A., Arziman, Z., Stempfle, D. et al. Dev. Cell, 18 (2010),pp. 862-876
[33]	Schubiger, M., Carre, C., Antoniewski, C. et al. Development, 132 (2005),pp. 5239-5248
[34]	Schubiger, M., Wade, A.A., Carney, G.E. et al. Development, 125 (1998),pp. 2053-2062
[35]	Sprinzak, D., Lakhanpal, A., Lebon, L. et al. Nature, 465 (2010),pp. 86-90
[36]	Thompson, B.J., Mathieu, J., Sung, H.H. et al. Dev. Cell, 9 (2005),pp. 711-720
[37]	Thummel, C.S. Trends Genet., 12 (1996),pp. 306-310
[38]	Xie, G., Yu, Z., Jia, D. et al. J. Cell Sci., 127 (2014),pp. 3830-3839
[39]	Xu, T., Rubin, G.M. Development, 117 (1993),pp. 1223-1237
[40]	Zacharioudaki, E., Bray, S.J. Methods, 68 (2014),pp. 173-182
[41]	Zhang, Q., Zhang, Y., Wu, L. et al. J. Genet. Genomics, 41 (2014),pp. 317-325
[42]	Zhou, X., Riddiford, L.M. Development, 129 (2002),pp. 2259-2269