A Subset of Drosophila Myc Sites Remain Associated with Mitotic Chromosomes Colocalized with Insulator Proteins

Overview

Journal Nat Commun

Specialty Biology

Date 2013 Feb 14

PMID 23403565

Citations 48

Authors

Jingping Yang

Elizabeth Sung

Paul G Donlin-Asp

Victor G Corces

Affiliations

Soon will be listed here.

Abstract

Myc has been characterized as a transcription factor that activates expression of genes involved in pluripotency and cancer, and as a component of the replication complex. Here we find that Myc is present at promoters and enhancers of Drosophila melanogaster genes during interphase. Myc colocalizes with Orc2, which is part of the prereplication complex, during G1. As is the case in mammals, Myc associates preferentially with paused genes, suggesting that it may also be involved in the release of RNA polymerase II from the promoter-proximal pausing in Drosophila. Interestingly, about 40% of Myc sites present in interphase persists during mitosis. None of the Myc mitotic sites correspond to enhancers, and only some correspond to promoters. The rest of the mitotic Myc sites overlap with binding sites for multiple insulator proteins that are also maintained in mitosis. These results suggest alternative mechanisms to explain the role of Myc in pluripotency and cancer.

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References

Lieberman-Aiden E, van Berkum N, Williams L, Imakaev M, Ragoczy T, Telling A . Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009; 326(5950):289-93. PMC: 2858594. DOI: 10.1126/science.1181369. View

Rahl P, Lin C, Seila A, Flynn R, McCuine S, Burge C . c-Myc regulates transcriptional pause release. Cell. 2010; 141(3):432-45. PMC: 2864022. DOI: 10.1016/j.cell.2010.03.030. View

Ji H, Wu G, Zhan X, Nolan A, Koh C, De Marzo A . Cell-type independent MYC target genes reveal a primordial signature involved in biomass accumulation. PLoS One. 2011; 6(10):e26057. PMC: 3198433. DOI: 10.1371/journal.pone.0026057. View

Chen Q, Shi X, Rudolph C, Yu Y, Zhang D, Zhao X . Recurrent trisomy and Robertsonian translocation of chromosome 14 in murine iPS cell lines. Chromosome Res. 2011; 19(7):857-68. DOI: 10.1007/s10577-011-9239-y. View

Blackwell T, Kretzner L, Blackwood E, Eisenman R, Weintraub H . Sequence-specific DNA binding by the c-Myc protein. Science. 1990; 250(4984):1149-51. DOI: 10.1126/science.2251503. View

Wolfer A, Ramaswamy S . MYC and metastasis. Cancer Res. 2011; 71(6):2034-7. PMC: 3089000. DOI: 10.1158/0008-5472.CAN-10-3776. View

Xu H, Handoko L, Wei X, Ye C, Sheng J, Wei C . A signal-noise model for significance analysis of ChIP-seq with negative control. Bioinformatics. 2010; 26(9):1199-204. DOI: 10.1093/bioinformatics/btq128. View

Frye M, Fisher A, Watt F . Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS One. 2007; 2(8):e763. PMC: 1945016. DOI: 10.1371/journal.pone.0000763. View

Pierce S, Yost C, Britton J, Loo L, Flynn E, Edgar B . dMyc is required for larval growth and endoreplication in Drosophila. Development. 2004; 131(10):2317-27. DOI: 10.1242/dev.01108. View

10.

Kidder B, Yang J, Palmer S . Stat3 and c-Myc genome-wide promoter occupancy in embryonic stem cells. PLoS One. 2008; 3(12):e3932. PMC: 2592696. DOI: 10.1371/journal.pone.0003932. View

11.

Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W . c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell. 2012; 151(1):68-79. PMC: 3471363. DOI: 10.1016/j.cell.2012.08.033. View

12.

Ohta S, Bukowski-Wills J, Sanchez-Pulido L, de Lima Alves F, Wood L, Chen Z . The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell. 2010; 142(5):810-21. PMC: 2982257. DOI: 10.1016/j.cell.2010.07.047. View

13.

Van Bortle K, Ramos E, Takenaka N, Yang J, Wahi J, Corces V . Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. Genome Res. 2012; 22(11):2176-87. PMC: 3483547. DOI: 10.1101/gr.136788.111. View

14.

Phillips J, Corces V . CTCF: master weaver of the genome. Cell. 2009; 137(7):1194-211. PMC: 3040116. DOI: 10.1016/j.cell.2009.06.001. View

15.

van Riggelen J, Yetil A, Felsher D . MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer. 2010; 10(4):301-9. DOI: 10.1038/nrc2819. View

16.

Maines J, Stevens L, Tong X, Stein D . Drosophila dMyc is required for ovary cell growth and endoreplication. Development. 2004; 131(4):775-86. DOI: 10.1242/dev.00932. View

17.

Louis S, Vermolen B, Garini Y, Young I, Guffei A, Lichtensztejn Z . c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci U S A. 2005; 102(27):9613-8. PMC: 1172233. DOI: 10.1073/pnas.0407512102. View

18.

Meyer N, Penn L . Reflecting on 25 years with MYC. Nat Rev Cancer. 2008; 8(12):976-90. DOI: 10.1038/nrc2231. View

19.

Aguda B, Kim Y, Piper-Hunter M, Friedman A, Marsh C . MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci U S A. 2008; 105(50):19678-83. PMC: 2598727. DOI: 10.1073/pnas.0811166106. View

20.

Perna D, Faga G, Verrecchia A, Gorski M, Barozzi I, Narang V . Genome-wide mapping of Myc binding and gene regulation in serum-stimulated fibroblasts. Oncogene. 2011; 31(13):1695-709. PMC: 3324106. DOI: 10.1038/onc.2011.359. View