Molecular dissection of cis-regulatory modules at the Drosophila bithorax complex reveals critical transcription factor signature motifs

Developmental Biology

Volumn 359, Issue 2, 2011, Pages 290-302

  Starr, Michael O ^a   Ho, Margaret C W ^a   Gunther, Eric J M ^a   Tu, Yen Kuei ^a   Shur, Andrey S ^a   Goetz, Sara E ^a   Borok, Matthew J ^a   Kang, Victoria ^a   Drewell, Robert A ^a  

^a HARVEY MUDD COLLEGE   (United States)

Author keywords

Bithorax complex; Cis regulation; Drosophila; Enhancer; Evolution; Homeotic gene; Transcription factor

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MOLESKIN; UNCLASSIFIED DRUG; ABD A PROTEIN, DROSOPHILA; ABD B PROTEINS, DROSOPHILA; ABD-A PROTEIN, DROSOPHILA; ABD-B PROTEINS, DROSOPHILA; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; UBX PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; BLASTODERM; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; GENE FREQUENCY; GENE MUTATION; HETEROZYGOSITY; MITOTIC RECOMBINATION; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE TENDON JUNCTION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SOMATIC CELL; TENDON; ANIMAL; ANIMAL EMBRYO; BINDING SITE; BIOLOGICAL MODEL; DROSOPHILA MELANOGASTER; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; PROTEIN BINDING; REGULATORY SEQUENCE; SPECIES DIFFERENCE;

DROSOPHILA MELANOGASTER;

ANIMALS; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NUCLEAR PROTEINS; NUCLEOTIDE MOTIFS; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 82455199114     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.07.028     Document Type: Article

References (51)

1. Akbari O.S., et al. Unraveling cis-regulatory mechanisms at the abdominal-A and Abdominal-B genes in the Drosophila bithorax complex. Dev. Biol. 2006, 293:294.
2. Arnone M.I., Davidson E.H. The hardwiring of development: organization and function of genomic regulatory systems. Development 1997, 124:1851-1864.
3. Arnosti D.N., et al. The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 1996, 122:205-214.
4. Bae E., et al. Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. PNAS 2002, 99:16847-16852.
5. Berman B.P., et al. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. PNAS 2002, 99:757-762.
6. Berman B.P., et al. Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol. 2004, 5:R61.
7. Bischof J., et al. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3312-3317.
8. Borok M.J., et al. Dissecting the regulatory switches of development: lessons from enhancer evolution in Drosophila. Development 2010, 137:5-13.
9. Bowler T., et al. Computational identification of Ftz/Ftz-F1 downstream target genes. Dev. Biol. 2006, 299:78-90.
10. Bradley R.K., et al. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol. 2010, 8:e1000343.
11. Busturia A., Bienz M. Silencers in abdominal-B, a homeotic Drosophila gene. EMBO J. 1993, 12:1415-1425.
12. Casares F., Sanchez-Herrero E. Regulation of the infraabdominal regions of the bithorax complex of Drosophila by gap genes. Development 1995, 121:1855-1866.
13. Celniker S.E., et al. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 1990, 9:4277-4286.
14. Consortium O.R.A. ORegAnno: an open-access community-driven resource for regulatory annotation. Nucleic Acids Res. 2008, 36:D107-D113.
15. Costas J., et al. Turnover of binding sites for transcription factors involved in early Drosophila development. Gene 2003, 310:215-220.
16. Crocker J., Erives A. A closer look at the eve stripe 2 enhancers of Drosophila and Themira. PLoS Genet. 2008, 4:e1000276.
17. Dermitzakis E.T., Clark A.G. Evolution of transcription factor binding sites in mammalian gene regulatory regions: conservation and turnover. Mol. Biol. Evol. 2002, 19:1114-1121.
18. Erives A., Levine M. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3851-3856.
19. Frazer K.A., et al. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004, 32:W273-W279.
20. Hare E.E., et al. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet. 2008, 4:e1000106.
21. Hertz G.Z., Stormo G.D. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 1999, 15:563-577.
22. Ho M.C., et al. Functional evolution of cis-regulatory modules at a homeotic gene in Drosophila. PLoS Genet. 2009, 5:e1000709.
23. Jacob F., Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 1961, 3:318-356.
24. Kent W.J., et al. The human genome browser at UCSC. Genome Res. 2002, 12:996-1006.
25. Levine M., Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151.
26. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
27. Li X.Y., et al. The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol. 2011, 12:R34.
28. Ludwig M.Z., et al. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 2000, 403:564-567.
29. Ludwig M.Z., Kreitman M. Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol. Biol. Evol. 1995, 12:1002-1011.
30. Ludwig M.Z., et al. Functional evolution of a cis-regulatory module. Public Libr. Sci. 2005, 3:588-598.
31. Ludwig M.Z., et al. Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 1998, 125:949-958.
32. Lusk R.W., Eisen M.B. Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet. 2010, 22:e1000829.
33. MacArthur S., et al. Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol. 2009, 10:R80.
34. Maeda R.K., Karch F. The ABC of the BX-C: the bithorax complex explained. Development 2006, 133:1413-1422.
35. Markstein M., et al. Genome-wide analysis of clustered dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:763-768.
36. Martin C.H., et al. Complete sequence of the bithorax complex of Drosophila. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:8398-8402.
37. Mihaly J., et al. Dissecting the regulatory landscape of the Abd-B gene of the bithorax complex. Development 2006, 133:2983-2993.
38. Palena C.M., et al. Positively charged residues at the N-terminal arm of the homeodomain are required for efficient DNA binding by homeodomain-leucine zipper proteins. J. Mol. Biol. 2001, 308:39-47.
39. Ptashne M. A Genetic Switch 2004, Cold Spring Harbor Laboratory Press. Third Edition: Phage Lambda Revisited.
40. Sanchez-Herrero E., et al. Genetic organization of Drosophila bithorax complex. Nature 1985, 313:108-113.
41. Shimell M.J., et al. Functional analysis of repressor binding sites in the iab-2 regulatory region of the abdominal-A homeotic gene. Dev. Biol. 2000, 218:38-52.
42. Shimell M.J., et al. Enhancer point mutation results in a homeotic transformation in Drosophila. Science 1994, 264:968-971.
43. Small S., et al. Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev. 1991, 5:827-839.
44. Suzuki T., et al. Segmentation gene product Fushi Tarazu is an LXXLL motif-dependent coactivator for orphan receptor FTZ-F1. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12403-12408.
45. Swanson C.I., et al. Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. Dev. Cell 2010, 18:359-370.
46. Thomas-Chollier M., et al. RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 2008, 36:W119-W127.
47. Vavouri T., Elgar G. Prediction of cis-regulatory elements using binding site matrices-the successes, the failures and the reasons for both. Curr. Opin. Genet. Dev. 2005, 15:395-402.
48. Wasserman W.W., Fickett J.W. Identification of regulatory regions which confer muscle-specific gene expression. J. Mol. Biol. 1998, 278:167-181.
49. Wittkopp P. Variable transcription factor binding: a mechanism of evolutionary change. PLoS Biol. 2010, 8:e1000342.
50. Wray G.A. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 2007, 8:206-216.
51. Zhou J., et al. Characterization of the transvection mediating region of the abdominal-B locus in Drosophila. Development 1999, 126:3057-3065.