Transcription of Bxd Noncoding RNAs Promoted by Trithorax Represses Ubx in Cis by Transcriptional Interference

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2006 Dec 19

PMID 17174895

Citations 141

Authors

Svetlana Petruk

Yurii Sedkov

Kristen M Riley

Jacob Hodgson

Francois Schweisguth

Susumu Hirose

James B Jaynes

Hugh W Brock

Alexander Mazo

Affiliations

Soon will be listed here.

Abstract

Much of the genome is transcribed into long noncoding RNAs (ncRNAs). Previous data suggested that bithoraxoid (bxd) ncRNAs of the Drosophila bithorax complex (BX-C) prevent silencing of Ultrabithorax (Ubx) and recruit activating proteins of the trithorax group (trxG) to their maintenance elements (MEs). We found that, surprisingly, Ubx and several bxd ncRNAs are expressed in nonoverlapping patterns in both embryos and imaginal discs, suggesting that transcription of these ncRNAs is associated with repression, not activation, of Ubx. Our data rule out siRNA or miRNA-based mechanisms for repression by bxd ncRNAs. Rather, ncRNA transcription itself, acting in cis, represses Ubx. The Trithorax complex TAC1 binds the Ubx coding region in nuclei expressing Ubx, and the bxd region in nuclei not expressing Ubx. We propose that TAC1 promotes the mosaic pattern of Ubx expression by facilitating transcriptional elongation of bxd ncRNAs, which represses Ubx transcription.

Citing Articles

Decoding subcellular RNA localization one molecule at a time.

Biayna J, Dumbovic G Genome Biol. 2025; 26(1):45.

PMID: 40033325 PMC: 11874642. DOI: 10.1186/s13059-025-03507-8.

A Synergistic, Cultivator Model of De Novo Gene Origination.

Lee U, Mozeika S, Zhao L Genome Biol Evol. 2024; 16(6).

PMID: 38748819 PMC: 11152449. DOI: 10.1093/gbe/evae103.

-regulatory modes of inactivation in butterfly forewings.

Tendolkar A, Mazo-Vargas A, Livraghi L, Hanly J, Van Horne K, Gilbert L Elife. 2024; 12.

PMID: 38261357 PMC: 10945631. DOI: 10.7554/eLife.90846.

Insights into Spt6: a histone chaperone that functions in transcription, DNA replication, and genome stability.

Miller C, Warner J, Winston F Trends Genet. 2023; 39(11):858-872.

PMID: 37481442 PMC: 10592469. DOI: 10.1016/j.tig.2023.06.008.

The conserved histone chaperone Spt6 is strongly required for DNA replication and genome stability.

Miller C, Winston F Cell Rep. 2023; 42(3):112264.

PMID: 36924499 PMC: 10106089. DOI: 10.1016/j.celrep.2023.112264.

References

Hodgson J, Argiropoulos B, Brock H . Site-specific recognition of a 70-base-pair element containing d(GA)(n) repeats mediates bithoraxoid polycomb group response element-dependent silencing. Mol Cell Biol. 2001; 21(14):4528-43. PMC: 87112. DOI: 10.1128/MCB.21.14.4528-4543.2001. View

Guenther M, Jenner R, Chevalier B, Nakamura T, Croce C, Canaani E . Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci U S A. 2005; 102(24):8603-8. PMC: 1150839. DOI: 10.1073/pnas.0503072102. View

Eddy S . Computational genomics of noncoding RNA genes. Cell. 2002; 109(2):137-40. DOI: 10.1016/s0092-8674(02)00727-4. View

Rank G, Prestel M, Paro R . Transcription through intergenic chromosomal memory elements of the Drosophila bithorax complex correlates with an epigenetic switch. Mol Cell Biol. 2002; 22(22):8026-34. PMC: 134728. DOI: 10.1128/MCB.22.22.8026-8034.2002. View

Hogga I, Karch F . Transcription through the iab-7 cis-regulatory domain of the bithorax complex interferes with maintenance of Polycomb-mediated silencing. Development. 2002; 129(21):4915-22. DOI: 10.1242/dev.129.21.4915. View

Bender W, Fitzgerald D . Transcription activates repressed domains in the Drosophila bithorax complex. Development. 2002; 129(21):4923-30. DOI: 10.1242/dev.129.21.4923. View

Beisel C, Imhof A, Greene J, Kremmer E, Sauer F . Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature. 2002; 419(6909):857-62. DOI: 10.1038/nature01126. View

Gottesman S . Stealth regulation: biological circuits with small RNA switches. Genes Dev. 2002; 16(22):2829-42. DOI: 10.1101/gad.1030302. View

Bae E, Calhoun V, Levine M, Lewis E, Drewell R . Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. Proc Natl Acad Sci U S A. 2002; 99(26):16847-52. PMC: 139232. DOI: 10.1073/pnas.222671299. View

10.

Hampsey M, Reinberg D . Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell. 2003; 113(4):429-32. DOI: 10.1016/s0092-8674(03)00360-x. View

11.

Shimojima T, Okada M, Nakayama T, Ueda H, Okawa K, Iwamatsu A . Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor. Genes Dev. 2003; 17(13):1605-16. PMC: 196133. DOI: 10.1101/gad.1086803. View

12.

Pallavi S, Shashidhara L . Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs. Development. 2003; 130(20):4931-41. DOI: 10.1242/dev.00719. View

13.

Smith S, Petruk S, Sedkov Y, Cho E, Tillib S, Canaani E . Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex. Nat Cell Biol. 2004; 6(2):162-7. DOI: 10.1038/ncb1088. View

14.

Hughes C, Rozenblatt-Rosen O, Milne T, Copeland T, Levine S, Lee J . Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell. 2004; 13(4):587-97. DOI: 10.1016/s1097-2765(04)00081-4. View

15.

Milne T, Dou Y, Martin M, Brock H, Roeder R, Hess J . MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci U S A. 2005; 102(41):14765-70. PMC: 1253553. DOI: 10.1073/pnas.0503630102. View

16.

Ronshaugen M, Biemar F, Piel J, Levine M, Lai E . The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev. 2005; 19(24):2947-52. PMC: 1315399. DOI: 10.1101/gad.1372505. View

17.

Sanchez-Elsner T, Gou D, Kremmer E, Sauer F . RETRACTED: Noncoding RNAs of trithorax response elements recruit Drosophila Ash1 to Ultrabithorax. Science. 2006; 311(5764):1118-23. DOI: 10.1126/science.1117705. View

18.

Grimaud C, Bantignies F, Pal-Bhadra M, Ghana P, Bhadra U, Cavalli G . RNAi components are required for nuclear clustering of Polycomb group response elements. Cell. 2006; 124(5):957-71. DOI: 10.1016/j.cell.2006.01.036. View

19.

Carthew R . Gene regulation by microRNAs. Curr Opin Genet Dev. 2006; 16(2):203-8. DOI: 10.1016/j.gde.2006.02.012. View

20.

Massirer K, Pasquinelli A . The evolving role of microRNAs in animal gene expression. Bioessays. 2006; 28(5):449-52. DOI: 10.1002/bies.20406. View