The Drosophila Enhancer of split Gene Complex: Architecture and Coordinate Regulation by Notch, Cohesin, and Polycomb Group Proteins

G3: Genes, Genomes, Genetics

Volumn 3, Issue 9, 2013, Pages 1785-1794

  Schaaf, Cheri A ^a   Misulovin, Ziva ^a   Gause, Maria ^a   Koenig, Amanda ^a   Dorsett, Dale ^a   Doisy, Edward A ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromator; Nipped B; Putzig; RNA polymerase; Suppressor of Hairless

Indexed keywords

COHESIN; NOTCH RECEPTOR; POLYCOMB GROUP PROTEIN; RNA POLYMERASE;

ARCHITECTURE; ARTICLE; CELL LINE; CHROMOSOME; CONFORMATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; DROSOPHILA; ENHANCER OF SPLIT GENE COMPLEX; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; COMPLEX FORMATION; ENHANCER REGION; GENE; GENE CONTROL; GENETIC TRANSCRIPTION; NONHUMAN; PROTEIN EXPRESSION; RNA SPLICING;

CHROMATOR; NIPPED-B; PUTZIG; RNA POLYMERASE; SUPPRESSOR OF HAIRLESS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES, INSECT; DROSOPHILA; DROSOPHILA PROTEINS; POLYCOMB-GROUP PROTEINS; PROTEIN BINDING; RECEPTORS, NOTCH; REPRESSOR PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84885756457     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.007534     Document Type: Article

References (51)

1. Bailey, A. M., and J. W. Posakony, 1995 Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev. 9: 2609-2622.
2. Chien, R., W. Zeng, A. R. Ball, and K. Yokomori, 2011a Cohesin: a critical chromatin organizer in mammalian gene regulation. Biochem. Cell. Biol. 89: 445-458.
3. Chien, R., W. Zeng, S. Kawauchi, M. A. Bender, R. Santos et al., 2011b Cohesin mediates chromatin interactions that regulate mammalian b-globin expression. J. Biol. Chem. 286: 17870-17878.
4. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner, 2002 Capturing chromosome conformation. Science 295: 1306-1311.
5. Delest, A., T. Sexton, and G. Cavalli, 2012 Polycomb: a paradigm for genome organization from one to three dimensions. Curr. Opin. Cell Biol. 24: 405-414.
6. Dorsett, D., 2011 Cohesin: genomic insights into controlling gene transcription and development. Curr. Opin. Genet. Dev. 21: 199-206.
7. Dorsett, D., and M. Merkenschlager, 2013 Cohesin at active genes: a unifying theme for cohesin and gene expression from model organisms to humans. Curr. Opin. Cell Biol. 25: 327-333.
8. Dorsett, D., and L. Ström, 2012 The ancient and evolving roles of cohesin in gene expression and DNA repair. Curr. Biol. 22: R240-R250.
9. Dorsett, D., J. C. Eissenberg, Z. Misulovin, A. Martens, B. Redding et al., 2005 Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. Development 132: 4743-4753.
10. Duncan, E. J., and P. K. Dearden, 2010 Evolution of a genomic regulatory domain: the role of gene co-option and gene duplication in the Enhancer of split complex. Genome Res. 20: 917-928.
11. Eggert, H., A. Gortchakov, and H. Saumweber, 2004 Identification of the Drosophila interband-specific protein Z4 as a DNA-binding zinc-finger protein determining chromosomal structure. J. Cell Sci. 117: 4253-4264.
12. Faure, A. J., D. Schmidt, S. Watt, P. C. Schwalie, M. D. Wilson et al., 2012 Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules. Genome Res. 22: 2163-2175.
13. Fay, A., Z. Misulovin, J. Li, C. A. Schaaf, M. Gause et al., 2011 Cohesin selectively binds and regulates genes with paused RNA polymerase. Curr. Biol. 21: 1624-1634.
14. Fischle, W., Y.Wang, S. A. Jacobs, Y. Kim, C. D. Allis et al., 2003 Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17: 1870-1881.
15. Fryer, C. J., E. Lamar, I. Turbachova, C. Kintner, and K. A. Jones, 2002 Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev. 16: 1397-1411.
16. Fryer, C. J., J. B. White, and K. A. Jones, 2004 Mastermind recruits CycC: CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol. Cell 16: 509-520.
17. Gause, M., H. A. Webber, Z. Misulovin, G. Haller, R. A. Rollins et al., 2008 Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117: 51-66.
18. Gortchakov, A. A., H. Eggert, M. Gan, J. Mattow, I. F. Zhimulev et al., 2005 Chriz, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes. Chromosoma 114: 54-66.
19. Guo, Y., K. Monahan, H. Wu, J. Gertz, K. E. Varley et al., 2012 CTCF/ cohesin-mediated DNA looping is required for protocadherin a promoter choice. Proc. Natl. Acad. Sci. USA 109: 21081-21086.
20. Horsfield, J. A., C. G. Print, and M. Mönnich, 2012 Diverse developmental disorders from the one ring: distinct molecular pathways underlie the cohesinopathies. Front. Genet. 3: 171.
21. Johnson, W. E., W. Li, C. A. Meyer, R. Gottardo, J. S. Carroll et al., 2006 Model-based analysis of tiling-arrays for ChIP-chip. Proc. Natl. Acad. Sci. USA 103: 12457-12462.
22. Kagey, M. H., J. J. Newman, S. Bilodeau, Y. Zhan, D. A. Orlando et al., 2010 Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
23. Kassis, J. A., and J. L. Brown, 2013 Polycomb group response elements in Drosophila and vertebrates. Adv. Genet. 81: 83-118.
24. Kawauchi, S., A. L. Calof, R. Santos, M. E. Lopez-Burks, C. M. Young et al., 2009 Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/2) mouse, a model of Cornelia de Lange Syndrome. PLoS Genet. 5: e1000650.
25. Krejcí, A., and S. Bray, 2007 Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev. 21: 1322-1327.
26. Kugler, S. J., and A. C. Nagel, 2007 putzig is required for cell proliferation and regulates notch activity in Drosophila. Mol. Biol. Cell 18: 3733-3740.
27. Lin, C. Y., J. Lovén, P. B. Rahl, R. M. Paranal, C. B. Burge et al., 2012 Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151: 56-67.
28. Liu, J., and I. D. Krantz, 2009 Cornelia de Lange syndrome, cohesin, and beyond. Clin. Genet. 76: 303-314.
29. Maeder, M. L., B. J. Polansky, B. E. Robson, and D. A. Eastman, 2007 Phylogenetic footprinting analysis in the upstream regulatory regions of the Drosophila enhancer of split genes. Genetics 177: 1377-1394.
30. Mannini, L., S. Menga, and A. Musio, 2010 The expanding universe of cohesin functions: a new genome stability caretaker involved in human disease and cancer. Hum. Mutat. 31: 623-630.
31. Merkenschlager, M., and D. T. Odom, 2013 CTCF and cohesin: linking gene regulatory elements with their targets. Cell 152: 1285-1297.
32. Misulovin, Z., Y. B. Schwartz, X. Y. Li, T. G. Kahn, M. Gause et al., 2008 Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117: 89-102.
33. modENCODE Consortium S. Roy, J. Ernst, P. V. Kharchenko, P. Kheradpour et al., 2010 Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1797.
34. Monahan, K., N. D. Rudnick, P. D. Kehayova, F. Pauli, K. M. Newberry et al., 2012 Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-a gene expression. Proc. Natl. Acad. Sci. USA 109: 9125-9130.
35. Nagel, A. C., and A. Preiss, 1999 Notchspl is deficient for inductive processes in the eye, and E(spl)D enhances split by interfering with proneural activity. Dev. Biol. 208: 406-415.
36. Nasmyth, K., 2011 Cohesin: a catenase with separate entry and exit gates? Nat. Cell Biol. 13: 1170-1177.
37. Nie, Z., G. Hu, G. Wei, K. Cui, A. Yamane et al., 2012 c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151: 68-79.
38. Penton, A. L., L. D. Leonard, and N. B. Spinner, 2012 Notch signaling in human development and disease. Semin. Cell Dev. Biol. 23: 450-457.
39. Phillips-Cremins, J. E., M. E. Sauria, A. Sanyal, T. I. Gerasimova, B. R. Lajoie et al., 2013 Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153: 1281-1295.
40. Rath, U., Y. Ding, H. Deng, H. Qi, X. Bao et al., 2006 The chromodomain protein, Chromator, interacts with JIL-1 kinase and regulates the structure of Drosophila polytene chromosomes. J. Cell Sci. 119: 2332-2341.
41. Remeseiro, S., and A. Losada, 2013 Cohesin, a chromatin engagement ring. Curr. Opin. Cell Biol. 25: 63-71.
42. Remeseiro, S., A. Cuadrado, G. Gómez-López, D. G. Pisano, and A. Losada, 2012 A unique role of cohesin-SA1 in gene regulation and development. EMBO J. 31: 2090-2102.
43. Rhodes, J. M., F. K. Bentley, C. G. Print, D. Dorsett, Z. Misulovin et al., 2010 Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. Dev. Biol. 344: 637-649.
44. Rollins, R. A., P. Morcillo, and D. Dorsett, 1999 Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152: 577-593.
45. Schaaf, C. A., Z. Misulovin, G. Sahota, A. M. Siddiqui, Y. B. Schwartz et al., 2009 Regulation of the Drosophila Enhancer of split and invected-engrailed gene complexes by sister chromatid cohesion proteins. PLoS ONE 4: e6202.
46. Schaaf, C. A., H. Kwak, A. Koenig, Z. Misulovin, D. W. Gohara et al., 2013a Genome-wide control of RNA polymerase II activity by cohesin. PLoS Genet. 9: e1003382.
47. Schaaf, C. A., Z. Misulovin, M. Gause, A. Koenig, D. W. Gohara et al., 2013b Cohesin and Polycomb proteins functionally interact to control transcription at silenced and active genes. PLoS Genet. 9: e1003560.
48. Schwartz, Y. B., T. G. Kahn, P. Stenberg, K. Ohno, R. Bourgon, and V. Pirrotta, 2010 Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 6: e1000805.
49. Schwartz, Y. B., D. Linder-Basso, P. V. Kharchenko, M. Y. Tolstorukov, M. Kim et al., 2012 Nature and function of insulator protein binding sites in the Drosophila genome. Genome Res. 22: 2188-2198.
50. Seitan, V. C., B. Hao, K. Tachibana-Konwalski, T. Lavagnolli, H. Mira-Bontenbal et al., 2011 A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation. Nature 476: 467-471.
51. Strübbe, G., C. Popp, A. Schmidt, A. Pauli, L. Ringrose et al., 2011 Polycomb purification by in vivo biotinylation tagging reveals cohesin and Trithorax group proteins as interaction partners. Proc. Natl. Acad. Sci. USA 108: 5572-5577.