Genes Regulating the Remote Wing Margin Enhancer in the Drosophila cut Locus

INVESTIGATIONS

Genes Regulating the Remote Wing Margin Enhancer in the Drosophila cut Locus

P. Morcillo, C. Rosen and D. Dorsett
Molecular Biology Program, Sloan-Kettering Institute for Cancer Research, Memorial Sloan-Kettering Cancer Center, New York, New York 10021

The mechanisms that allow enhancers to activate promoters from thousands of base pairs away are disrupted by the suppressor of Hairy-wing protein (SUHW) of Drosophila. SUHW binds a DNA sequence in the gypsy retrotransposon and prevents enhancers promoter-distal to a gypsy insertion in a gene from activating without affecting promoter-proximal enhancers. Several observations indicate that SUHW does not affect enhancer-binding activators. Instead, SUHW may interfere with factors that structurally facilitate interactions between an enhancer and promoter. To identify putative enhancer facilitators, a screen for mutations that reduce activity of the remote wing margin enhancer in the cut gene was performed. Mutations in scalloped, mastermind, and a previously unknown gene, Chip, were isolated. A TEA DNA-binding domain in the Scalloped protein binds the wing margin enhancer. Interactions between scalloped, mastermind and Chip mutations indicate that mastermind and Chip act synergistically with scalloped to regulate the wing margin enhancer. Chip is essential and also affects expression of a gypsy insertion in Ultrabithorax. Relative to mutations in scalloped or mastermind, a Chip mutation hypersensitizes the wing margin enhancer in cut to gypsy insertions. Therefore, Chip might encode a target of SUHW enhancer-blocking activity.

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				P. Heitzler, L. Vanolst, I. Biryukova, and P. Ramain Enhancer-promoter communication mediated by Chip during Pannier-driven proneural patterning is regulated by Osa Genes & Dev., March 1, 2003; 17(5): 591 - 596. [Abstract] [Full Text] [PDF]

				M. Mukhopadhyay, A. Teufel, T. Yamashita, A. D. Agulnick, L. Chen, K. M. Downs, A. Schindler, A. Grinberg, S.-P. Huang, D. Dorward, et al. Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation Development, February 1, 2003; 130(3): 495 - 505. [Abstract] [Full Text] [PDF]

				L. Chen, D. Segal, N. A. Hukriede, A. V. Podtelejnikov, D. Bayarsaihan, J. A. Kennison, V. V. Ogryzko, I. B. Dawid, and H. Westphal Ssdp proteins interact with the LIM-domain-binding protein Ldb1 to regulate development PNAS, October 29, 2002; 99(22): 14320 - 14325. [Abstract] [Full Text] [PDF]

				A. G. West, M. Gaszner, and G. Felsenfeld Insulators: many functions, many mechanisms Genes & Dev., February 1, 2002; 16(3): 271 - 288. [Full Text] [PDF]

				M. Gause, P. Morcillo, and D. Dorsett Insulation of Enhancer-Promoter Communication by a Gypsy Transposon Insert in the Drosophila cut Gene: Cooperation between Suppressor of Hairy-wing and Modifier of mdg4 Proteins Mol. Cell. Biol., July 15, 2001; 21(14): 4807 - 4817. [Abstract] [Full Text] [PDF]

				D. van Meyel, D. O'Keefe, S Thor, L. Jurata, G. Gill, and J. Thomas Chip is an essential cofactor for apterous in the regulation of axon guidance in Drosophila Development, January 5, 2000; 127(9): 1823 - 1831. [Abstract] [PDF]

				M. Bulger and M. Groudine Looping versus linking: toward a model for long-distance gene activation Genes & Dev., October 1, 1999; 13(19): 2465 - 2477. [Full Text]

				S. M. Jackson and C. A. Berg Soma-to-Germline Interactions During Drosophila Oogenesis Are Influenced by Dose-Sensitive Interactions Between cut and the Genes cappuccino, ovarian tumor and agnostic Genetics, September 1, 1999; 153(1): 289 - 303. [Abstract] [Full Text]

				R. A. Rollins, P. Morcillo, and D. Dorsett Nipped-B, a Drosophila Homologue of Chromosomal Adherins, Participates in Activation by Remote Enhancers in the cut and Ultrabithorax Genes Genetics, June 1, 1999; 152(2): 577 - 593. [Abstract] [Full Text]

				A. Golovnin, M. Gause, S. Georgieva, E. Gracheva, and P. Georgiev The su(Hw) Insulator Can Disrupt Enhancer-Promoter Interactions When Located More than 20 Kilobases Away from the Drosophila achaete-scute Complex Mol. Cell. Biol., May 1, 1999; 19(5): 3443 - 3456. [Abstract] [Full Text] [PDF]

				J. R. Morris, J.-l. Chen, S. T. Filandrinos, R. C. Dunn, R. Fisk, P. K. Geyer, and C.-t. Wu An Analysis of Transvection at the yellow Locus of Drosophila melanogaster Genetics, February 1, 1999; 151(2): 633 - 651. [Abstract] [Full Text]

				P Ligoxygakis, S. Bray, Y Apidianakis, and C Delidakis Ectopic expression of individual E(spl) genes has differential effects on different cell fate decisions and underscores the biphasic requirement for notch activity in wing margin establishment in Drosophila Development, January 5, 1999; 126(10): 2205 - 2214. [Abstract] [PDF]

				A. J. Simmonds, X. Liu, K. H. Soanes, H. M. Krause, K. D. Irvine, and J. B. Bell Molecular interactions between Vestigial and Scalloped promote wing formation in Drosophila Genes & Dev., December 15, 1998; 12(24): 3815 - 3820. [Abstract] [Full Text]

				J. R. Morris, J.-l. Chen, P. K. Geyer, and C.-t. Wu Two modes of transvection: Enhancer action in trans and bypass of a chromatin insulator in cis PNAS, September 1, 1998; 95(18): 10740 - 10745. [Abstract] [Full Text] [PDF]

				M. Gause, H. Hovhannisyan, T. Kan, S. Kuhfittig, V. Mogila, and P. Georgiev hobo Induced Rearrangements in the yellow Locus Influence the Insulation Effect of the gypsy su(Hw)-Binding Region in Drosophila melanogaster Genetics, July 1, 1998; 149(3): 1393 - 1405. [Abstract] [Full Text] [PDF]

				P. Morcillo, C. Rosen, M. K. Baylies, and D. Dorsett Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila Genes & Dev., October 15, 1997; 11(20): 2729 - 2740. [Abstract] [Full Text] [PDF]

				C. Micchelli, E. Rulifson, and S. Blair The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate Development, January 4, 1997; 124(8): 1485 - 1495. [Abstract] [PDF]

				E. Torigoi, I. M. Bennani-Baiti, C. Rosen, K. Gonzalez, P. Morcillo, M. Ptashne, and D. Dorsett Chip interacts with diverse homeodomain proteins and potentiates Bicoid activity in vivo PNAS, March 14, 2000; 97(6): 2686 - 2691. [Abstract] [Full Text] [PDF]