Dynamic Control of Enhancer Repertoires Drives Lineage and Stage-Specific Transcription during Hematopoiesis

Developmental Cell

Volumn 36, Issue 1, 2016, Pages 9-23

  Huang, Jialiang ^b,c   Liu, Xin ^a   Li, Dan ^d   Shao, Zhen ^e   Cao, Hui ^a   Zhang, Yuannyu ^a,e   Trompouki, Eirini ^b,g   Bowman, Teresa V ^b,h   Zon, Leonard I ^b,f   Yuan, Guo Cheng ^c   Orkin, Stuart H ^b,f   Xu, Jian ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d HARVARD COLLEGE   (United States)

^e Chinese Academy of Sciences   (China)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^h ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; CHROMATIN; GATA1 PROTEIN, HUMAN; GATA2 PROTEIN, HUMAN;

ADULT; ARTICLE; CELL LINEAGE; CHROMATIN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENHANCER REGION; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; FETUS; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA EDITING; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN; GATA1 TRANSCRIPTION FACTOR; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; TRANSCRIPTION FACTORS;

EID: 84958739420     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.12.014     Document Type: Article

References (59)

1. Abraham B.J., Cui K., Tang Q., Zhao K. Dynamic regulation of epigenomic landscapes during hematopoiesis. BMC Genomics 2013, 14:193.
2. Amigo J.D., Yu M., Troadec M.B., Gwynn B., Cooney J.D., Lambert A.J., Chi N.C., Weiss M.J., Peters L.L., Kaplan J., et al. Identification of distal cis-regulatory elements at mouse mitoferrin loci using zebrafish transgenesis. Mol. Cell. Biol. 2011, 31:1344-1356.
3. Andersson R., Gebhard C., Miguel-Escalada I., Hoof I., Bornholdt J., Boyd M., Chen Y., Zhao X., Schmidl C., Suzuki T., et al. An atlas of active enhancers across human cell types and tissues. Nature 2014, 507:455-461.
4. Babu M.M., Luscombe N.M., Aravind L., Gerstein M., Teichmann S.A. Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 2004, 14:283-291.
5. Banerji J., Rusconi S., Schaffner W. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 1981, 27:299-308.
6. Bauer D.E., Kamran S.C., Lessard S., Xu J., Fujiwara Y., Lin C., Shao Z., Canver M.C., Smith E.C., Pinello L., et al. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level. Science 2013, 342:253-257.
7. Beck D., Thoms J.A., Perera D., Schutte J., Unnikrishnan A., Knezevic K., Kinston S.J., Wilson N.K., O'Brien T.A., Gottgens B., et al. Genome-wide analysis of transcriptional regulators in human HSPCs reveals a densely interconnected network of coding and noncoding genes. Blood 2013, 122:e12-22.
8. Bresnick E.H., Lee H.Y., Fujiwara T., Johnson K.D., Keles S. GATA switches as developmental drivers. J. Biol. Chem. 2010, 285:31087-31093.
9. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 2012, 28:276-284.
10. Bulger M., Groudine M. Functional and mechanistic diversity of distal transcription enhancers. Cell 2011, 144:327-339.
11. Cantor A.B., Orkin S.H. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 2002, 21:3368-3376.
12. Canver M.C., Smith E.C., Sher F., Pinello L., Sanjana N.E., Shalem O., Chen D.D., Schupp P.G., Vinjamur D.S., Garcia S.P., et al. BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis. Nature 2015, 527:192-197.
13. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
14. Dogan N., Wu W., Morrissey C.S., Chen K.B., Stonestrom A., Long M., Keller C.A., Cheng Y., Jain D., Visel A., et al. Occupancy by key transcription factors is a more accurate predictor of enhancer activity than histone modifications or chromatin accessibility. Epigenetics Chromatin 2015, 8:16.
15. Dore L.C., Chlon T.M., Brown C.D., White K.P., Crispino J.D. Chromatin occupancy analysis reveals genome-wide GATA factor switching during hematopoiesis. Blood 2012, 119:3724-3733.
16. ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
17. Espin-Palazon R., Stachura D.L., Campbell C.A., Garcia-Moreno D., Del Cid N., Kim A.D., Candel S., Meseguer J., Mulero V., Traver D. Proinflammatory signaling regulates hematopoietic stem cell emergence. Cell 2014, 159:1070-1085.
18. Groschel S., Sanders M.A., Hoogenboezem R., de Wit E., Bouwman B.A., Erpelinck C., van der Velden V.H., Havermans M., Avellino R., van Lom K., et al. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell 2014, 157:369-381.
19. He Q., Zhang C., Wang L., Zhang P., Ma D., Lv J., Liu F. Inflammatory signaling regulates hematopoietic stem and progenitor cell emergence in vertebrates. Blood 2015, 125:1098-1106.
20. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
21. Heintzman N.D., Hon G.C., Hawkins R.D., Kheradpour P., Stark A., Harp L.F., Ye Z., Lee L.K., Stuart R.K., Ching C.W., et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
22. Hnisz D., Abraham B.J., Lee T.I., Lau A., Saint-Andre 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.
23. Hnisz D., Schuijers J., Lin C.Y., Weintraub A.S., Abraham B.J., Lee T.I., Bradner J.E., Young R.A. Convergence of developmental and oncogenic signaling pathways at transcriptional super-enhancers. Mol. Cell 2015, 58:362-370.
24. Kaneko H., Shimizu R., Yamamoto M. GATA factor switching during erythroid differentiation. Curr. Opin. Hematol. 2010, 17:163-168.
25. Li Y., Esain V., Teng L., Xu J., Kwan W., Frost I.M., Yzaguirre A.D., Cai X., Cortes M., Maijenburg M.W., et al. Inflammatory signaling regulates embryonic hematopoietic stem and progenitor cell production. Genes Dev. 2014, 28:2597-2612.
26. Loven J., Hoke H.A., Lin C.Y., Lau A., Orlando D.A., Vakoc C.R., Bradner J.E., Lee T.I., Young R.A. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013, 153:320-334.
27. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
28. Mansour M.R., Abraham B.J., Anders L., Berezovskaya A., Gutierrez A., Durbin A.D., Etchin J., Lawton L., Sallan S.E., Silverman L.B., et al. Oncogene regulation. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science 2014, 346:1373-1377.
29. Mathelier A., Zhao X., Zhang A.W., Parcy F., Worsley-Hunt R., Arenillas D.J., Buchman S., Chen C.Y., Chou A., Ienasescu H., et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014, 42:D142-D147.
30. McCall M.N., Jaffee H.A., Zelisko S.J., Sinha N., Hooiveld G., Irizarry R.A., Zilliox M.J. The Gene Expression Barcode 3.0: improved data processing and mining tools. Nucleic Acids Res. 2014, 42:D938-D943.
31. McLean C.Y., Bristor D., Hiller M., Clarke S.L., Schaar B.T., Lowe C.B., Wenger A.M., Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 2010, 28:495-501.
32. Neph S., Vierstra J., Stergachis A.B., Reynolds A.P., Haugen E., Vernot B., Thurman R.E., John S., Sandstrom R., Johnson A.K., et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 2012, 489:83-90.
33. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
34. Parker S.C., Stitzel M.L., Taylor D.L., Orozco J.M., Erdos M.R., Akiyama J.A., van Bueren K.L., Chines P.S., Narisu N., Black B.L., et al. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc. Natl. Acad. Sci. USA 2013, 110:17921-17926.
35. Pennacchio L.A., Bickmore W., Dean A., Nobrega M.A., Bejerano G. Enhancers: five essential questions. Nat. Rev. Genet. 2013, 14:288-295.
36. Pinello L., Xu J., Orkin S.H., Yuan G.C. Analysis of chromatin-state plasticity identifies cell-type-specific regulators of H3K27me3 patterns. Proc. Natl. Acad. Sci. USA 2014, 111:E344-E353.
37. Pott S., Lieb J.D. What are super-enhancers?. Nat. Genet. 2015, 47:8-12.
38. Rolland T., Tasan M., Charloteaux B., Pevzner S.J., Zhong Q., Sahni N., Yi S., Lemmens I., Fontanillo C., Mosca R., et al. A proteome-scale map of the human interactome network. Cell 2014, 159:1212-1226.
39. Sankaran V.G., Xu J., Ragoczy T., Ippolito G.C., Walkley C.R., Maika S.D., Fujiwara Y., Ito M., Groudine M., Bender M.A., et al. Developmental and species-divergent globin switching are driven by BCL11A. Nature 2009, 460:1093-1097.
40. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
41. Shao Z., Zhang Y., Yuan G.C., Orkin S.H., Waxman D.J. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets. Genome Biol. 2012, 13:R16.
42. Shaw G.C., Cope J.J., Li L., Corson K., Hersey C., Ackermann G.E., Gwynn B., Lambert A.J., Wingert R.A., Traver D., et al. Mitoferrin is essential for erythroid iron assimilation. Nature 2006, 440:96-100.
43. Snow J.W., Trowbridge J.J., Fujiwara T., Emambokus N.E., Grass J.A., Orkin S.H., Bresnick E.H. A single cis element maintains repression of the key developmental regulator Gata2. PLoS Genet. 2010, 6:e1001103.
44. Snow J.W., Trowbridge J.J., Johnson K.D., Fujiwara T., Emambokus N.E., Grass J.A., Orkin S.H., Bresnick E.H. Context-dependent function of "GATA switch" sites in vivo. Blood 2011, 117:4769-4772.
45. Su M.Y., Steiner L.A., Bogardus H., Mishra T., Schulz V.P., Hardison R.C., Gallagher P.G. Identification of biologically relevant enhancers in human erythroid cells. J. Biol. Chem. 2013, 288:8433-8444.
46. Szklarczyk D., Franceschini A., Wyder S., Forslund K., Heller D., Huerta-Cepas J., Simonovic M., Roth A., Santos A., Tsafou K.P., et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015, 43:D447-D452.
47. Trompouki E., Bowman T.V., Lawton L.N., Fan Z.P., Wu D.C., DiBiase A., Martin C.S., Cech J.N., Sessa A.K., Leblanc J.L., et al. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 2011, 147:577-589.
48. Tsai F.Y., Keller G., Kuo F.C., Weiss M., Chen J., Rosenblatt M., Alt F.W., Orkin S.H. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994, 371:221-226.
49. Van Handel B., Prashad S.L., Hassanzadeh-Kiabi N., Huang A., Magnusson M., Atanassova B., Chen A., Hamalainen E.I., Mikkola H.K. The first trimester human placenta is a site for terminal maturation of primitive erythroid cells. Blood 2010, 116:3321-3330.
50. Vaquerizas J.M., Kummerfeld S.K., Teichmann S.A., Luscombe N.M. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 2009, 10:252-263.
51. Visel A., Bristow J., Pennacchio L.A. Enhancer identification through comparative genomics. Semin. Cell. Dev. Biol. 2007, 18:140-152.
52. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
53. Visel A., Rubin E.M., Pennacchio L.A. Genomic views of distant-acting enhancers. Nature 2009, 461:199-205.
54. Welch J.J., Watts J.A., Vakoc C.R., Yao Y., Wang H., Hardison R.C., Blobel G.A., Chodosh L.A., Weiss M.J. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 2004, 104:3136-3147.
55. 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.
56. Wilson N.K., Foster S.D., Wang X., Knezevic K., Schutte J., Kaimakis P., Chilarska P.M., Kinston S., Ouwehand W.H., Dzierzak E., et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010, 7:532-544.
57. Xu J., Smale S.T. Designing an enhancer landscape. Cell 2012, 151:929-931.
58. Xu J., Shao Z., Glass K., Bauer D.E., Pinello L., Van Handel B., Hou S., Stamatoyannopoulos J.A., Mikkola H.K., Yuan G.C., et al. Combinatorial assembly of developmental stage-specific enhancers controls gene expression programs during human erythropoiesis. Dev. Cell 2012, 23:796-811.
59. Xu J., Shao Z., Li D., Xie H., Kim W., Huang J., Taylor J.E., Pinello L., Glass K., Jaffe J.D., et al. Developmental control of polycomb subunit composition by GATA factors mediates a switch to non-canonical functions. Mol. Cell 2015, 57:304-316.