Development, Vol 113, Issue 3 735-747, Copyright © 1991 by Company of Biologists

JOURNAL ARTICLES

Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer

J Jack, D Dorsett, Y Delotto and S Liu
Molecular Biology Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10021.

The cut locus is a complex gene whose function is necessary for specification of a number of cell types, including the external sensory organs. The cut wing class of mutations of the cut locus are homozygous viable and lack tissue from the wing margin, which is normally composed of external sensory organs and noninnervated bristles. Expression of cut was examined in the developing wings of wild-type and mutant pupae using an antiserum against Cut protein. Cut is expressed in all of the external sensory organs of the wing and the noninnervated bristles of the posterior margin. The cut wing class of mutations prevents Cut expression specifically in the wing margin mechanoreceptors and noninnervated bristles, apparently preventing neural differentiation. The transformed cells die soon after differentiation would have occurred. We identify an enhancer, located about 80 kb upstream of the cut gene promoter, that confers expression in the cells of the mechanoreceptors and noninnervated bristles from a heterologous promoter. The 27 gypsy retrotransposon insertions that prevent expression in these margin cells, all occur between this enhancer and the promoter. These gypsy insertions probably interfere with the interaction between the enhancer and the cut gene promoter.

This article has been cited by other articles:

				C. Cadieux, R. Harada, M. Paquet, O. Cote, M. Trudel, A. Nepveu, and M. Bouchard Polycystic Kidneys Caused by Sustained Expression of Cux1 Isoform p75 J. Biol. Chem., May 16, 2008; 283(20): 13817 - 13824. [Abstract] [Full Text] [PDF]

				A. Golovnin, A. Mazur, M. Kopantseva, M. Kurshakova, P. V. Gulak, B. Gilmore, W. G. F. Whitfield, P. Geyer, V. Pirrotta, and P. Georgiev Integrity of the Mod(mdg4)-67.2 BTB Domain Is Critical to Insulator Function in Drosophila melanogaster Mol. Cell. Biol., February 1, 2007; 27(3): 963 - 974. [Abstract] [Full Text] [PDF]

				A. M. Lee and C.-t. Wu Enhancer-Promoter Communication at the yellow Gene of Drosophila melanogaster: Diverse Promoters Participate in and Regulate trans Interactions Genetics, December 1, 2006; 174(4): 1867 - 1880. [Abstract] [Full Text] [PDF]

				H. Jafar-Nejad, A.-C. Tien, M. Acar, and H. J. Bellen Senseless and Daughterless confer neuronal identity to epithelial cells in the Drosophila wing margin Development, May 1, 2006; 133(9): 1683 - 1692. [Abstract] [Full Text] [PDF]

				M. Gause, J. C. Eissenberg, A. F. MacRae, M. Dorsett, Z. Misulovin, and D. Dorsett Nipped-A, the Tra1/TRRAP Subunit of the Drosophila SAGA and Tip60 Complexes, Has Multiple Roles in Notch Signaling during Wing Development. Mol. Cell. Biol., March 1, 2006; 26(6): 2347 - 2359. [Abstract] [Full Text] [PDF]

				L. Sansregret, B. Goulet, R. Harada, B. Wilson, L. Leduy, J. Bertoglio, and A. Nepveu The p110 Isoform of the CDP/Cux Transcription Factor Accelerates Entry into S Phase. Mol. Cell. Biol., March 1, 2006; 26(6): 2441 - 2455. [Abstract] [Full Text] [PDF]

				D. Dorsett, J. C. Eissenberg, Z. Misulovin, A. Martens, B. Redding, and K. McKim Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila Development, November 1, 2005; 132(21): 4743 - 4753. [Abstract] [Full Text] [PDF]

				J. J. Krupp, L. E. Yaich, R. J. Wessells, and R. Bodmer Identification of Genetic Loci That Interact With cut During Drosophila Wing-Margin Development Genetics, August 1, 2005; 170(4): 1775 - 1795. [Abstract] [Full Text] [PDF]

				G. Yang, Y.-H. Lee, Y. Jiang, X. Shi, S. Kertbundit, and T. C. Hall A Two-Edged Role for the Transposable Element Kiddo in the rice ubiquitin2 Promoter PLANT CELL, May 1, 2005; 17(5): 1559 - 1568. [Abstract] [Full Text] [PDF]

				M. Truscott, L. Raynal, Y. Wang, G. Berube, L. Leduy, and A. Nepveu The N-terminal Region of the CCAAT Displacement Protein (CDP)/Cux Transcription Factor Functions as an Autoinhibitory Domain that Modulates DNA Binding J. Biol. Chem., November 26, 2004; 279(48): 49787 - 49794. [Abstract] [Full Text] [PDF]

				R. A. Rollins, M. Korom, N. Aulner, A. Martens, and D. Dorsett Drosophila Nipped-B Protein Supports Sister Chromatid Cohesion and Opposes the Stromalin/Scc3 Cohesion Factor To Facilitate Long-Range Activation of the cut Gene Mol. Cell. Biol., April 15, 2004; 24(8): 3100 - 3111. [Abstract] [Full Text] [PDF]

				M. Shimizu, A. Takeshita, T. Tsukamoto, F. J. Gonzalez, and T. Osumi Tissue-Selective, Bidirectional Regulation of PEX11{alpha} and Perilipin Genes through a Common Peroxisome Proliferator Response Element Mol. Cell. Biol., February 1, 2004; 24(3): 1313 - 1323. [Abstract] [Full Text] [PDF]

				P. Giraldo, A. Martinez, L. Regales, A. Lavado, A. Garcia-Diaz, A. Alonso, A. Busturia, and L. Montoliu Functional dissection of the mouse tyrosinase locus control region identifies a new putative boundary activity Nucleic Acids Res., November 1, 2003; 31(21): 6290 - 6305. [Abstract] [Full Text] [PDF]

				M. Truscott, L. Raynal, P. Premdas, B. Goulet, L. Leduy, G. Berube, and A. Nepveu CDP/Cux Stimulates Transcription from the DNA Polymerase {alpha} Gene Promoter Mol. Cell. Biol., April 15, 2003; 23(8): 3013 - 3028. [Abstract] [Full Text] [PDF]

				B. Goulet, P. Watson, M. Poirier, L. Leduy, G. Berube, S. Meterissian, P. Jolicoeur, and A. Nepveu Characterization of a Tissue-specific CDP/Cux Isoform, p75, Activated in Breast Tumor Cells Cancer Res., November 15, 2002; 62(22): 6625 - 6633. [Abstract] [Full Text] [PDF]

				F. Boudreau, E. H. H. M. Rings, G. P. Swain, A. M. Sinclair, E. R. Suh, D. G. Silberg, R. H. Scheuermann, and P. G. Traber A Novel Colonic Repressor Element Regulates Intestinal Gene Expression by Interacting with Cux/CDP Mol. Cell. Biol., August 1, 2002; 22(15): 5467 - 5478. [Abstract] [Full Text] [PDF]

				J. C. Eissenberg, J. Ma, M. A. Gerber, A. Christensen, J. A. Kennison, and A. Shilatifard dELL is an essential RNA polymerase II elongation factor with a general role in development PNAS, July 23, 2002; 99(15): 9894 - 9899. [Abstract] [Full Text] [PDF]

				M. X. Luong, C. M. van der Meijden, D. Xing, R. Hesselton, E. S. Monuki, S. N. Jones, J. B. Lian, J. L. Stein, G. S. Stein, E. J. Neufeld, et al. Genetic Ablation of the CDP/Cux Protein C Terminus Results in Hair Cycle Defects and Reduced Male Fertility Mol. Cell. Biol., March 1, 2002; 22(5): 1424 - 1437. [Abstract] [Full Text] [PDF]

				A. M. Sinclair, J. A. Lee, A. Goldstein, D. Xing, S. Liu, R. Ju, P. W. Tucker, E. J. Neufeld, and R. H. Scheuermann Lymphoid apoptosis and myeloid hyperplasia in CCAAT displacement protein mutant mice Blood, December 15, 2001; 98(13): 3658 - 3667. [Abstract] [Full Text] [PDF]

				M. Santaguida, Q. Ding, G. Berube, M. Truscott, P. Whyte, and A. Nepveu Phosphorylation of the CCAAT Displacement Protein (CDP)/Cux Transcription Factor by Cyclin A-Cdk1 Modulates Its DNA Binding Activity in G2 J. Biol. Chem., November 30, 2001; 276(49): 45780 - 45790. [Abstract] [Full Text] [PDF]

				N. S. Moon, P. Premdas, M. Truscott, L. Leduy, G. Berube, and A. Nepveu S Phase-Specific Proteolytic Cleavage Is Required To Activate Stable DNA Binding by the CDP/Cut Homeodomain Protein Mol. Cell. Biol., September 15, 2001; 21(18): 6332 - 6345. [Abstract] [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]

				E. Muravyova, A. Golovnin, E. Gracheva, A. Parshikov, T. Belenkaya, V. Pirrotta, and P. Georgiev Loss of Insulator Activity by Paired Su(Hw) Chromatin Insulators Science, January 19, 2001; 291(5503): 495 - 498. [Abstract] [Full Text]

				R. Nolo, L. A. Abbott, and H. J. Bellen Drosophila Lyra Mutations Are Gain-of-Function Mutations of senseless Genetics, January 1, 2001; 157(1): 307 - 315. [Abstract] [Full Text]

				A. Tavares, T Tsukui, and J. Izpisua Belmonte Evidence that members of the Cut/Cux/CDP family may be involved in AER positioning and polarizing activity during chick limb development Development, January 12, 2000; 127(23): 5133 - 5144. [Abstract] [PDF]

				J. de Celis and S. Bray The Abruptex domain of Notch regulates negative interactions between Notch, its ligands and Fringe Development, January 3, 2000; 127(6): 1291 - 1302. [Abstract] [PDF]

				L. Girard and M. Freeling Mutator-Suppressible Alleles of rough sheath1 and liguleless3 in Genetics, January 1, 2000; 154(1): 437 - 446. [Abstract] [Full Text]

				K. C. Scott, A. D. Taubman, and P. K. Geyer Enhancer Blocking by the Drosophila gypsy Insulator Depends Upon Insulator Anatomy and Enhancer Strength Genetics, October 1, 1999; 153(2): 787 - 798. [Abstract] [Full Text] [PDF]

				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]

				I. D. Zorin, T. I. Gerasimova, and V. G. Corces The lawc Gene Is a New Member of the trithorax-Group That Affects the Function of the gypsy Insulator of Drosophila Genetics, July 1, 1999; 152(3): 1045 - 1055. [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]

				A. Soldatov, E. Nabirochkina, S. Georgieva, T. Belenkaja, and P. Georgiev TAFII40 Protein Is Encoded by the e(y)1 Gene: Biological Consequences of Mutations Mol. Cell. Biol., May 1, 1999; 19(5): 3769 - 3778. [Abstract] [Full Text] [PDF]

				S. Li, L. Moy, N. Pittman, G. Shue, B. Aufiero, E. J. Neufeld, N. S. LeLeiko, and M. J. Walsh Transcriptional Repression of the Cystic Fibrosis Transmembrane Conductance Regulator Gene, Mediated by CCAAT Displacement Protein/cut Homolog, Is Associated with Histone Deacetylation J. Biol. Chem., March 19, 1999; 274(12): 7803 - 7815. [Abstract] [Full Text] [PDF]

				R Nagaraj, A. Pickup, R Howes, K Moses, M Freeman, and U Banerjee Role of the EGF receptor pathway in growth and patterning of the Drosophila wing through the regulation of vestigial Development, January 2, 1999; 126(5): 975 - 985. [Abstract] [PDF]

				G. Halder, P. Polaczyk, M. E. Kraus, A. Hudson, J. Kim, A. Laughon, and S. Carroll The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila Genes & Dev., December 15, 1998; 12(24): 3900 - 3909. [Abstract] [Full Text]

				B. H. Judd Genes and Chromomeres: A Puzzle in Three Dimensions Genetics, September 1, 1998; 150(1): 1 - 9. [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]

				O. Coqueret, N. Martin, G. Berube, M. Rabbat, D. W. Litchfield, and A. Nepveu DNA Binding by Cut Homeodomain Proteins Is Down-modulated by Casein Kinase II J. Biol. Chem., January 30, 1998; 273(5): 2561 - 2566. [Abstract] [Full Text] [PDF]

				G Campbell and A Tomlinson The roles of the homeobox genes aristaless and Distal-less in patterning the legs and wings of Drosophila Development, January 11, 1998; 125(22): 4483 - 4493. [Abstract] [PDF]

				Polycomb Group Repression Is Blocked by the Drosophila suppressor of Hairy-wing [su(Hw)] Insulator Genetics, January 1, 1998; 148(1): 331 - 340.

				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]

				A Majumdar, R Nagaraj, and U Banerjee strawberry notch encodes a conserved nuclear protein that functions downstream of Notch and regulates gene expression along the developing wing margin of Drosophila. Genes & Dev., May 15, 1997; 11(10): 1341 - 1353. [Abstract] [PDF]

				D. A. Shelton, L. Stegman, R. Hardison, W. Miller, J. H. Bock, J. L. Slightom, M. Goodman, and D. L. Gumucio Phylogenetic Footprinting of Hypersensitive Site 3 of the beta -Globin Locus Control Region Blood, May 1, 1997; 89(9): 3457 - 3469. [Abstract] [Full Text] [PDF]

				L. A. Dickinson, C. D. Dickinson, and T. Kohwi-Shigematsu An Atypical Homeodomain in SATB1 Promotes Specific Recognition of the Key Structural Element in a Matrix Attachment Region J. Biol. Chem., April 25, 1997; 272(17): 11463 - 11470. [Abstract] [Full Text] [PDF]

				J. de Celis and S Bray Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing Development, January 9, 1997; 124(17): 3241 - 3251. [Abstract] [PDF]

				S. Jackson and K Blochlinger cut interacts with Notch and protein kinase A to regulate egg chamber formation and to maintain germline cyst integrity during Drosophila oogenesis Development, January 9, 1997; 124(18): 3663 - 3672. [Abstract] [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]

				O. Coqueret, G. Berube, and A. Nepveu DNA Binding by Cut Homeodomain Proteins Is Down-modulated by Protein Kinase C J. Biol. Chem., October 4, 1996; 271(40): 24862 - 24868. [Abstract] [Full Text] [PDF]

				W. Luo and D. G. Skalnik CCAAT Displacement Protein Competes with Multiple Transcriptional Activators for Binding to Four Sites in the Proximal gp91phox Promoter J. Biol. Chem., July 26, 1996; 271(30): 18203 - 18210. [Abstract] [Full Text] [PDF]

				C. Neumann and S. Cohen A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing Development, January 11, 1996; 122(11): 3477 - 3485. [Abstract] [PDF]

				J. de Celis, A Garcia-Bellido, and S. Bray Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc Development, January 1, 1996; 122(1): 359 - 369. [Abstract] [PDF]

				R. Roseman, J. Swan, and P. Geyer A Drosophila insulator protein facilitates dosage compensation of the X chromosome min-white gene located at autosomal insertion sites Development, January 11, 1995; 121(11): 3573 - 3582. [Abstract] [PDF]

				J. de Celis, M Llimargas, and J Casanova Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster Development, January 10, 1995; 121(10): 3405 - 3416. [Abstract] [PDF]

				M Vervoort, D Zink, N Pujol, K Victoir, N Dumont, A Ghysen, and C Dambly-Chaudiere Genetic determinants of sense organ identity in Drosophila: regulatory interactions between cut and poxn Development, January 9, 1995; 121(9): 3111 - 3120. [Abstract] [PDF]

				V Andres, M D Chiara, and V Mahdavi A new bipartite DNA-binding domain: cooperative interaction between the cut repeat and homeo domain of the cut homeo proteins. Genes & Dev., January 15, 1994; 8(2): 245 - 257. [Abstract] [PDF]

				S. Blair, D. Brower, J. Thomas, and M Zavortink The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila Development, January 7, 1994; 120(7): 1805 - 1815. [Abstract] [PDF]

				J. Couso, S. Bishop, and A Martinez Arias The wingless signalling pathway and the patterning of the wing margin in Drosophila Development, January 3, 1994; 120(3): 621 - 636. [Abstract] [PDF]

				D A Harrison, D A Gdula, R S Coyne, and V G Corces A leucine zipper domain of the suppressor of Hairy-wing protein mediates its repressive effect on enhancer function. Genes & Dev., October 1, 1993; 7(10): 1966 - 1978. [Abstract] [PDF]

				S. Blair Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila Development, January 10, 1993; 119(2): 339 - 351. [Abstract] [PDF]

				R. Phillips and J. Whittle wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development Development, January 6, 1993; 118(2): 427 - 438. [Abstract] [PDF]

				K Blochlinger, L. Jan, and Y. Jan Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila Development, January 2, 1993; 117(2): 441 - 450. [Abstract] [PDF]

				P K Geyer and V G Corces DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes & Dev., October 1, 1992; 6(10): 1865 - 1873. [Abstract] [PDF]