Engrailed cooperates directly with Extradenticle and Homothorax on a distinct class of homeodomain binding sites to repress sloppy paired

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 382-392

  Fujioka, Miki ^a   Gebelein, Brian ^b   Cofer, Zenobia C ^a   Mann, Richard S ^c   Jaynes, James B ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Cooperative homeoprotein sites; Engrailed; Extradenticle; Homeodomain protein binding; Homothorax; Sloppy paired

Indexed keywords

EXTRADENTICLE PROTEIN; HOMEODOMAIN PROTEIN; HOMOTHORAX PROTEIN; HOX PROTEIN; TRANSCRIPTION FACTOR ENGRAILED; TRANSCRIPTION FACTOR EVEN SKIPPED; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BLASTODERM; CELL EXPANSION; CIS REGULATORY MODULE; CONTROLLED STUDY; DNA STRUCTURE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

EID: 84861222971     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.04.004     Document Type: Article

References (47)

1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development 1987, 101:1-22.
2. Alexandre C., Vincent J.P. Requirements for transcriptional repression and activation by Engrailed in Drosophila embryos. Development 2003, 130:729-739.
3. Bateman J.R., Lee A.M., Wu C.T. Site-specific transformation of Drosophila via phiC31 integrase-mediated cassette exchange. Genetics 2006, 173:769-777.
4. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 2007, 104:3312-3317.
5. Brody T., Rasband W., Baler K., Kuzin A., Kundu M., Odenwald W.F. Sequence conservation and combinatorial complexity of Drosophila neural precursor cell enhancers. BMC Genomics 2008, 9:371.
6. Cadigan K.M., Grossniklaus U., Gehring W.J. Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev. 1994, 8:899-913.
7. Carey M. The enhanceosome and transcriptional synergy. Cell 1998, 92:5-8.
8. Celniker S.E., Dillon L.A.L., Gerstein M.B., Gunsalus K.C., Henikoff S., Karpen G.H., Kellis M., Lai E.C., Lieb J.D., MacAlpine D.M., Micklem G., Piano F., Snyder M., Stein L., White K.P., Waterston R.H., mod E.C. Unlocking the secrets of the genome. Nature 2009, 459:927-930.
9. Choe C.P., Brown S.J. Evolutionary flexibility of pair-rule patterning revealed by functional analysis of secondary pair-rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum. Dev. Biol. 2007, 302:281-294.
10. Clark A.G., Eisen M.B., Smith D.R., Bergman C.M., Oliver B., Markow T.A. et al., Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450:203-218.
11. Datta R.R., Small S. Gene regulation: piecing together the puzzle of enhancer evolution. Curr. Biol. 2011, 21:R542-543.
12. Frankel N., Davis G.K., Vargas D., Wang S., Payre F., Stern D.L. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 2010, 466:490-493.
13. Frasch M., Hoey T., Rushlow C., Doyle H., Levine M. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 1987, 6:749-759.
14. Frasch M., Warrior R., Tugwood J., Levine M. Molecular analysis of even-skipped mutants in Drosophila development. Genes Dev. 1988, 2:1824-1838.
15. Fujioka M., Jaynes J.B. Regulation of a duplicated locus: Drosophila sloppy paired is replete with functionally overlapping enhancers. Dev. Biol. 2012, 362:309-319.
16. Fujioka M., Jaynes J.B., Goto T. Early even-skipped stripes act as morphogenetic gradients at the single cell level to establish engrailed expression. Development 1995, 121:4371-4382.
17. Fujioka M., Lear B.C., Landgraf M., Yusibova G.L., Zhou J., Riley K.M., Patel N.H., Jaynes J.B. Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 2003, 130:5385-5400.
18. Fujioka M., Yusibova G.L., Patel N.H., Brown S.J., Jaynes J.B. The repressor activity of even-skipped is highly conserved, and is sufficient to activate engrailed and to regulate both the spacing and stability of parasegment boundaries. Development 2002, 129:4411-4421.
19. Fujioka M., Yusibova G.L., Zhou J., Jaynes J.B. The DNA-binding Polycomb-group protein Pleiohomeotic maintains both active and repressed transcriptional states through a single site. Development 2008, 135:4131-4139.
20. Gebelein B., Culi J., Ryoo H.D., Zhang W., Mann R.S. Specificity of Distalless repression and limb primordia development by abdominal Hox proteins. Dev. Cell 2002, 3:487-498.
21. Gebelein B., McKay D.J., Mann R.S. Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 2004, 431:653-659.
22. Grossniklaus U., Pearson R.K., Gehring W.J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 1992, 6:1030-1051.
23. Groth A.C., Fish M., Nusse R., Calos M.P. Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 2004, 166:1775-1782.
24. Heemskerk J., DiNardo S., Kostriken R., O'Farrell P.H. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 1991, 352:404-410.
25. Hoey T., Levine M. Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature 1988, 332:858-861.
26. Ingham P.W., Gergen J.P. Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo. Development 1988, 104:51-60. (Supplement).
27. Jaynes J.B., Fujioka M. Drawing lines in the sand: even skipped et al. and parasegment boundaries (erratum appears in Dev. Biol. 2004 Aug 1;272(1):277-8). Dev. Biol. 2004, 269:609-622.
28. Jaynes J.B., O'Farrell P.H. Active repression of transcription by the engrailed homeodomain protein. EMBO J. 1991, 10:1427-1433.
29. Kobayashi M., Fujioka M., Tolkunova E.N., Deka D., Abu-Shaar M., Mann R.S., Jaynes J.B. Engrailed cooperates with extradenticle and homothorax to repress target genes in Drosophila. Development 2003, 130:741-751.
30. Kosman D., Mizutani C.M., Lemons D., Cox W.G., McGinnis W., Bier E. Multiplex detection of RNA expression in Drosophila embryos. Science 2004, 305:846.
31. Kuzin A., Kundu M., Ekatomatis A., Brody T., Odenwald W.F. Conserved sequence block clustering and flanking inter-cluster flexibility delineate enhancers that regulate nerfin-1 expression during Drosophila CNS development. Gene Expression Patterns 2009, 9:65-72.
32. Lelli K.M., Noro B., Mann R.S. Variable motif utilization in homeotic selector (Hox)-cofactor complex formation controls specificity. Proc. Natl. Acad. Sci. USA 2011, 108:21122-21127.
33. Macdonald P.M., Ingham P., Struhl G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell 1986, 47:721-734.
34. Mann R.S., Lelli K.M., Joshi R. Hox specificity unique roles for cofactors and collaborators. Curr. Top. Dev. Biol. 2009, 88:63-101.
35. Manoukian A.S., Krause H.M. Control of segmental asymmetry in Drosophila embryos. Development 1993, 118:785-796.
36. Negre N., Brown C.D., Ma L., Bristow C.A., Miller S.W., Wagner U., Kheradpour P., Eaton M.L., Loriaux P., Sealfon R., Li Z., Ishii H., Spokony R.F., Chen J., Hwang L., Cheng C., Auburn R.P., Davis M.B., Domanus M., Shah P.K., Morrison C.A., Zieba J., Suchy S., Senderowicz L., Victorsen A., Bild N.A., Grundstad A.J., Hanley D., MacAlpine D.M., Mannervik M., Venken K., Bellen H., White R., Gerstein M., Russell S., Grossman R.L., Ren B., Posakony J.W., Kellis M., White K.P. A cis-regulatory map of the Drosophila genome. Nature 2011, 471:527-531.
37. Odenwald W.F., Rasband W., Kuzin A., Brody T. EVOPRINTER, a multigenomic comparative tool for rapid identification of functionally important DNA. Proc. Natl. Acad. Sci. USA 2005, 102:14700-14705.
38. Peifer M., Wieschaus E. Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev. 1990, 4:1209-1223.
39. Perry M.W., Boettiger A.N., Bothma J.P., Levine M. Shadow enhancers foster robustness of Drosophila gastrulation. Curr. Biol. 2010, 20:1562-1567.
40. Prazak L., Fujioka M., Gergen J.P. Non-additive interactions involving two distinct elements mediate sloppy-paired regulation by pair-rule transcription factors. Dev. Biol. 2010, 344:1048-1059.
41. Riechmann V., Irion U., Wilson R., Grosskortenhaus R., Leptin M. Control of cell fates and segmentation in the Drosophila mesoderm. Development 1997, 124:2915-2922.
42. Rieckhof G.E., Casares F., Ryoo H.D., Abu-Shaar M., Mann R.S. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 1997, 91:171-183.
43. Slattery M., Riley T., Liu P., Abe N., Gomez-Alcala P., Dror I., Zhou T., Rohs R., Honig B., Bussemaker H.J., Mann R.S. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 2011, 147:1270-1282.
44. Struhl G. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature 1985, 318:677-680.
45. Tolkunova E.N., Fujioka M., Kobayashi M., Deka D., Jaynes J.B. Two distinct types of repression domain in engrailed: one interacts with the groucho corepressor and is preferentially active on integrated target genes. Mol. Cell. Biol. 1998, 18:2804-2814.
46. Uhl J.D., Cook T.A., Gebelein B. Comparing anterior and posterior Hox complex formation reveals guidelines for predicting cis-regulatory elements. Dev. Biol. 2010, 343:154-166.
47. Zhang S., Xu L., Lee J., Xu T. Drosophila atrophin homolog functions as a transcriptional corepressor in multiple developmental processes. Cell 2002, 108:45-56.