Combgap contributes to recruitment of Polycomb group proteins in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 14, 2016, Pages 3826-3831

  Ray, Payal ^a   De, Sandip ^a   Mitra, Apratim ^a   Bezstarosti, Karel ^b   Demmers, Jeroen A A ^b   Pfeifer, Karl ^a   Kassis, Judith A ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Combgap; Gene expression; PcG recruitment; Polycomb; PREs

Indexed keywords

BMI1 PROTEIN; DNA BINDING PROTEIN; PLEIOHOMEOTIC PROTEIN; POLYCOMB GROUP PROTEIN; POLYHOMEOTIC PROTEIN; UNCLASSIFIED DRUG; COMBGAP PROTEIN, DROSOPHILA; DNA; DROSOPHILA PROTEIN; PHO PROTEIN, DROSOPHILA; POLYCOMB PROTEIN, DROSOPHILA; POLYHOMEOTIC PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENOME; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; ANIMAL; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE MOTIF;

ANIMALS; BINDING SITES; CELL DIFFERENTIATION; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NUCLEOTIDE MOTIFS; POLYCOMB REPRESSIVE COMPLEX 1; POLYCOMB-GROUP PROTEINS; TRANSCRIPTION FACTORS;

EID: 84962638112     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1520926113     Document Type: Article

References (49)

1. Lanzuolo C, Orlando V (2012) Memories from the polycomb group proteins. Annu Rev Genet 46:561-589.
2. Di Croce L, Helin K (2013) Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20(10):1147-1155.
3. Simon JA, Kingston RE (2013) Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 49(5):808-824.
4. Bracken AP, Helin K (2009) Polycomb group proteins: Navigators of lineage pathways led astray in cancer. Nat Rev Cancer 9(11):773-784.
5. Kassis JA, Brown JL (2013) Polycomb group response elements in Drosophila and vertebrates. Adv Genet 81:83-118.
6. Steffen PA, Ringrose L (2014) What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat Rev Mol Cell Biol 15(5):340-356.
7. van Kruijsbergen I, Hontelez S, Veenstra GJ (2015) Recruiting polycomb to chromatin. Int J Biochem Cell Biol 67:177-187.
8. Simon J, Chiang A, Bender W, Shimell MJ, O'Connor M (1993) Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev Biol 158(1):131-144.
9. Zink B, Engström Y, Gehring WJ, Paro R (1991) Direct interaction of the Polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J 10(1):153-162.
10. Chan CS, Rastelli L, Pirrotta V (1994) A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J 13(11): 2553-2564.
11. Chiang A, O'Connor MB, Paro R, Simon J, Bender W (1995) Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development 121(6): 1681-1689.
12. Schwartz YB, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38(6):700-705.
13. Tolhuis B, et al. (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38(6):694-699.
14. Schuettengruber B, et al. (2009) Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol 7(1):e13.
15. Ringrose L, Rehmsmeier M, Dura JM, Paro R (2003) Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev Cell 5(5): 759-771.
16. Hauenschild A, Ringrose L, Altmutter C, Paro R, Rehmsmeier M (2008) Evolutionary plasticity of polycomb/trithorax response elements in Drosophila species. PLoS Biol 6(10):e261.
17. Fiedler T, Rehmsmeier M (2006) jPREdictor: A versatile tool for the prediction of cisregulatory elements. Nucleic Acids Res 34(Web Server issue):W546-50.
18. Zeng J, Kirk BD, Gou Y, Wang Q, Ma J (2012) Genome-wide polycomb target gene prediction in Drosophila melanogaster. Nucleic Acids Res 40(13):5848-5863.
19. Brown JL, Kassis JA (2013) Architectural and functional diversity of polycomb group response elements in Drosophila. Genetics 195(2):407-419.
20. Klymenko T, et al. (2006) A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev 20(9):1110-1122.
21. Fritsch C, Brown JL, Kassis JA, Müller J (1999) The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 126(17): 3905-3913.
22. Kozma G, Bender W, Sipos L (2008) Replacement of a Drosophila Polycomb response element core, and in situ analysis of its DNA motifs. Mol Genet Genomics 279(6): 595-603.
23. Brown JL, Fritsch C, Mueller J, Kassis JA (2003) The Drosophila pho-like gene encodes a YY1-related DNA binding protein that is redundant with pleiohomeotic in homeotic gene silencing. Development 130(2):285-294.
24. Kahn TG, Stenberg P, Pirrotta V, Schwartz YB (2014) Combinatorial interactions are required for the efficient recruitment of pho repressive complex (PhoRC) to polycomb response elements. PLoS Genet 10(7):e1004495.
25. Orsi GA, et al. (2014) High-resolution mapping defines the cooperative architecture of Polycomb response elements. Genome Res 24(5):809-820.
26. Déjardin J, et al. (2005) Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature 434(7032):533-538.
27. Blastyák A, Mishra RK, Karch F, Gyurkovics H (2006) Efficient and specific targeting of Polycomb group proteins requires cooperative interaction between Grainyhead and Pleiohomeotic. Mol Cell Biol 26(4):1434-1444.
28. Chang YL, King B, Lin SC, Kennison JA, Huang DH (2007) A double-bromodomain protein, FSH-S, activates the homeotic gene ultrabithorax through a critical promoter-proximal region. Mol Cell Biol 27(15):5486-5498.
29. Brown JL, Kassis JA (2010) Spps, a Drosophila Sp1/KLF family member, binds to PREs and is required for PRE activity late in development. Development 137(15):2597-2602.
30. Americo J, et al. (2002) A complex array of DNA-binding proteins required for pairingsensitive silencing by a polycomb group response element from the Drosophila engrailed gene. Genetics 160(4):1561-1571.
31. Okulski H, Druck B, Bhalerao S, Ringrose L (2011) Quantitative analysis of polycomb response elements (PREs) at identical genomic locations distinguishes contributions of PRE sequence and genomic environment. Epigenetics Chromatin 4:4.
32. Campbell GL, Tomlinson A (2000) Transcriptional regulation of the Hedgehog effector CI by the zinc-finger gene combgap. Development 127(19):4095-4103.
33. Svendsen PC, Marshall SD, Kyba M, Brook WJ (2000) The combgap locus encodes a zinc-finger protein that regulates cubitus interruptus during limb development in Drosophila melanogaster. Development 127(19):4083-4093.
34. Emerson RO, Thomas JH (2009) Adaptive evolution in zinc finger transcription factors. PLoS Genet 5(1):e1000325.
35. Chanas G, Lavrov S, Iral F, Cavalli G, Maschat F (2004) Engrailed and polyhomeotic maintain posterior cell identity through cubitus-interruptus regulation. Dev Biol 272(2): 522-535.
36. Song Y, Chung S, Kunes S (2000) Combgap relays wingless signal reception to the determination of cortical cell fate in the Drosophila visual system. Mol Cell 6(5):1143-1154.
37. Machanick P, Bailey TL (2011) MEME-ChIP: Motif analysis of large DNA datasets. Bioinformatics 27(12):1696-1697.
38. Williams JA, Bell JB, Carroll SB (1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5(12B):2481-2495.
39. Williams JA, Paddock SW, Vorwerk K, Carroll SB (1994) Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. Nature 368(6469):299-305.
40. Lee N, Maurange C, Ringrose L, Paro R (2005) Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature 438(7065):234-237.
41. dos Santos G, et al.; Fly Base Consortium (2015) Fly Base: Introduction of the Drosophila melanogaster Release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Res 43(Database issue):D690-D697.
42. Kang H, et al. (2015) Sex comb on midleg (Scm) is a functional link between PcGrepressive complexes in Drosophila. Genes Dev 29(11):1136-1150.
43. Schaaf CA, et al. (2013) Cohesin and polycomb proteins functionally interact to control transcription at silenced and active genes. PLoS Genet 9(6):e1003560.
44. Soto MC, Chou TB, Bender W (1995) Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 140(1):231-243.
45. Kennison JA (1995) The Polycomb and trithorax group proteins of Drosophila: Transregulators of homeotic gene function. Annu Rev Genet 29:289-303.
46. Schuettengruber B, et al. (2014) Cooperativity, specificity, and evolutionary stability of Polycomb targeting in Drosophila. Cell Reports 9(1):219-233.
47. Franza BR, Jr, Josephs SF, Gilman MZ, Ryan W, Clarkson B (1987) Characterization of cellular proteins recognizing the HIV enhancer using a microscale DNA-affinity precipitation assay. Nature 330(6146):391-395.
48. Langlais KK, Brown JL, Kassis JA (2012) Polycomb group proteins bind an engrailed PRE in both the "ON" and "OFF" transcriptional states of engrailed. PLoS One 7(11): e48765.
49. Mohd-Sarip A, Venturini F, Chalkley GE, Verrijzer CP (2002) Pleiohomeotic can link polycomb to DNA and mediate transcriptional repression. Mol Cell Biol 22(21): 7473-7483.