Active and Inactive Enhancers Cooperate to Exert Localized and Long-Range Control of Gene Regulation

Cell Reports

Volumn 15, Issue 10, 2016, Pages 2159-2169

  Proudhon, Charlotte ^a   Snetkova, Valentina ^a   Raviram, Ramya ^a,b   Lobry, Camille ^a,f   Badri, Sana ^a,b   Jiang, Tingting ^c   Hao, Bingtao ^a   Trimarchi, Thomas ^a   Kluger, Yuval ^c   Aifantis, Iannis ^a   Bonneau, Richard ^b,d,e   Skok, Jane A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY   (United States)

^e Simons Center for Data Analysis   (United States)

^f INSERM   (France)

Author keywords

Enhancer sharing; Gene regulation; Igk; Localized and long range contacts; Nuclear architecture; Super enhancer; Tcrb; Transcription factor binding; Transcriptional output

Indexed keywords

CORE BINDING FACTOR BETA; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CHROMATIN; CONTROLLED STUDY; ENHANCER REGION; GENE; GENE CONTROL; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; IGK GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY SEQUENCE; T LYMPHOCYTE; TCRB GENE; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM;

ANIMALS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; MICE, INBRED C57BL; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 84969801874     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.087     Document Type: Article

References (41)

1. Alt F.W., Zhang Y., Meng F.L., Guo C., Schwer B. Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 2013, 152:417-429.
2. Anders S., Pyl P.T., Huber W. HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31:166-169.
3. Bories J.C., Demengeot J., Davidson L., Alt F.W. Gene-targeted deletion and replacement mutations of the T-cell receptor beta-chain enhancer: the role of enhancer elements in controlling V(D)J recombination accessibility. Proc. Natl. Acad. Sci. USA 1996, 93:7871-7876.
4. Bouvier G., Watrin F., Naspetti M., Verthuy C., Naquet P., Ferrier P. Deletion of the mouse T-cell receptor beta gene enhancer blocks alphabeta T-cell development. Proc. Natl. Acad. Sci. USA 1996, 93:7877-7881.
5. Buenrostro J.D., Giresi P.G., Zaba L.C., Chang H.Y., Greenleaf W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 2013, 10:1213-1218.
6. Cheutin T., Cavalli G. Progressive polycomb assembly on H3K27me3 compartments generates polycomb bodies with developmentally regulated motion. PLoS Genet. 2012, 8:e1002465.
7. Collins A., Hewitt S.L., Chaumeil J., Sellars M., Micsinai M., Allinne J., Parisi F., Nora E.P., Bolland D.J., Corcoran A.E., et al. RUNX transcription factor-mediated association of Cd4 and Cd8 enables coordinate gene regulation. Immunity 2011, 34:303-314.
8. Dryden N.H., Broome L.R., Dudbridge F., Johnson N., Orr N., Schoenfelder S., Nagano T., Andrews S., Wingett S., Kozarewa I., et al. Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi-C. Genome Res. 2014, 24:1854-1868.
9. Fuxa M., Skok J., Souabni A., Salvagiotto G., Roldan E., Busslinger M. Pax5 induces V-to-DJ rearrangements and locus contraction of the immunoglobulin heavy-chain gene. Genes Dev. 2004, 18:411-422.
10. Goldmit M., Ji Y., Skok J., Roldan E., Jung S., Cedar H., Bergman Y. Epigenetic ontogeny of the Igk locus during B cell development. Nat. Immunol. 2005, 6:198-203.
11. Hewitt S.L., Farmer D., Marszalek K., Cadera E., Liang H.E., Xu Y., Schlissel M.S., Skok J.A. Association between the Igk and Igh immunoglobulin loci mediated by the 3' Igk enhancer induces 'decontraction' of the Igh locus in pre-B cells. Nat. Immunol. 2008, 9:396-404.
12. Hewitt S.L., Yin B., Ji Y., Chaumeil J., Marszalek K., Tenthorey J., Salvagiotto G., Steinel N., Ramsey L.B., Ghysdael J., et al. RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci. Nat. Immunol. 2009, 10:655-664.
13. Hnisz D., Abraham B.J., Lee T.I., Lau A., Saint-André V., Sigova A.A., Hoke H.A., Young R.A. Super-enhancers in the control of cell identity and disease. Cell 2013, 155:934-947.
14. Inlay M., Alt F.W., Baltimore D., Xu Y. Essential roles of the kappa light chain intronic enhancer and 3' enhancer in kappa rearrangement and demethylation. Nat. Immunol. 2002, 3:463-468.
15. Inlay M.A., Tian H., Lin T., Xu Y. Important roles for E protein binding sites within the immunoglobulin kappa chain intronic enhancer in activating Vkappa Jkappa rearrangement. J. Exp. Med. 2004, 200:1205-1211.
16. Inlay M.A., Lin T., Gao H.H., Xu Y. Critical roles of the immunoglobulin intronic enhancers in maintaining the sequential rearrangement of IgH and Igk loci. J. Exp. Med. 2006, 203:1721-1732.
17. Johnson K., Chaumeil J., Skok J.A. Epigenetic regulation of V(D)J recombination. Essays Biochem. 2010, 48:221-243.
18. Kosak S.T., Skok J.A., Medina K.L., Riblet R., Le Beau M.M., Fisher A.G., Singh H. Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 2002, 296:158-162.
19. Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9:357-359.
20. Lara-Astiaso D., Weiner A., Lorenzo-Vivas E., Zaretsky I., Jaitin D.A., David E., Keren-Shaul H., Mildner A., Winter D., Jung S., et al. Immunogenetics. Chromatin state dynamics during blood formation. Science 2014, 345:943-949.
21. Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15:550.
22. Majumder K., Koues O.I., Chan E.A., Kyle K.E., Horowitz J.E., Yang-Iott K., Bassing C.H., Taniuchi I., Krangel M.S., Oltz E.M. Lineage-specific compaction of Tcrb requires a chromatin barrier to protect the function of a long-range tethering element. J. Exp. Med. 2015, 212:107-120.
23. McCarthy M.T., O'Callaghan C.A. PeaKDEck: a kernel density estimator-based peak calling program for DNaseI-seq data. Bioinformatics 2014, 30:1302-1304.
24. Pierce J.W., Gifford A.M., Baltimore D. Silencing of the expression of the immunoglobulin kappa gene in non-B cells. Mol. Cell. Biol. 1991, 11:1431-1437.
25. Pott S., Lieb J.D. What are super-enhancers?. Nat. Genet. 2015, 47:8-12.
26. Proudhon C., Hao B., Raviram R., Chaumeil J., Skok J.A. Long-range regulation of V(D)J recombination. Adv. Immunol. 2015, 128:123-182.
27. Qian J., Wang Q., Dose M., Pruett N., Kieffer-Kwon K.R., Resch W., Liang G., Tang Z., Mathé E., Benner C., et al. B cell super-enhancers and regulatory clusters recruit AID tumorigenic activity. Cell 2014, 159:1524-1537.
28. Raviram R., Rocha P.P., Müller C.L., Miraldi E.R., Badri S., Fu Y., Swanzey E., Proudhon C., Snetkova V., Bonneau R., Skok J.A. 4C-ker: a method to reproducibly identify genome-wide interactions captured by 4C-seq experiments. PLoS Comput. Biol. 2016, 12:e1004780.
29. Roldán E., Fuxa M., Chong W., Martinez D., Novatchkova M., Busslinger M., Skok J.A. Locus 'decontraction' and centromeric recruitment contribute to allelic exclusion of the immunoglobulin heavy-chain gene. Nat. Immunol. 2005, 6:31-41.
30. Sayegh C.E., Jhunjhunwala S., Riblet R., Murre C. Visualization of looping involving the immunoglobulin heavy-chain locus in developing B cells. Genes Dev. 2005, 19:322-327.
31. Schatz D.G., Swanson P.C. V(D)J recombination: mechanisms of initiation. Annu. Rev. Genet. 2011, 45:167-202.
32. Schoenfelder S., Sexton T., Chakalova L., Cope N.F., Horton A., Andrews S., Kurukuti S., Mitchell J.A., Umlauf D., Dimitrova D.S., et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 2010, 42:53-61.
33. Setoguchi R., Tachibana M., Naoe Y., Muroi S., Akiyama K., Tezuka C., Okuda T., Taniuchi I. Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development. Science 2008, 319:822-825.
34. Skok J.A., Gisler R., Novatchkova M., Farmer D., de Laat W., Busslinger M. Reversible contraction by looping of the Tcra and Tcrb loci in rearranging thymocytes. Nat. Immunol. 2007, 8:378-387.
35. Sun L., Zhang Z., Bailey T.L., Perkins A.C., Tallack M.R., Xu Z., Liu H. Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinformatics 2012, 13:331.
36. Trimarchi T., Bilal E., Ntziachristos P., Fabbri G., Dalla-Favera R., Tsirigos A., Aifantis I. Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia. Cell 2014, 158:593-606.
37. van de Werken H.J., Landan G., Holwerda S.J., Hoichman M., Klous P., Chachik R., Splinter E., Valdes-Quezada C., Oz Y., Bouwman B.A., et al. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat. Methods 2012, 9:969-972.
38. Whyte W.A., Orlando D.A., Hnisz D., Abraham B.J., Lin C.Y., Kagey M.H., Rahl P.B., Lee T.I., Young R.A. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
39. Yancopoulos G.D., Alt F.W. Developmentally controlled and tissue-specific expression of unrearranged VH gene segments. Cell 1985, 40:271-281.
40. Zhang Y., Liu T., Meyer C.A., Eeckhoute J., Johnson D.S., Bernstein B.E., Nusbaum C., Myers R.M., Brown M., Li W., Liu X.S. Model-based analysis of ChIP-seq (MACS). Genome Biol. 2008, 9:R137.
41. Zhou X., Xiang Y., Garrard W.T. The Igκ gene enhancers, E3' and Ed, are essential for triggering transcription. J. Immunol. 2010, 185:7544-7552.