DNA methylation dynamics during intestinal stem cell differentiation reveals enhancers driving gene expression in the villus

Genome Biology

Volumn 14, Issue 5, 2013, Pages

  Kaaij, Lucas T J ^a   van de Wetering, Marc ^a   Fang, Fang ^c   Decato, Benjamin ^c   Molaro, Antoine ^b   van de Werken, Harmen J G ^a   van Es, Johan H ^a   Schuijers, Jurian ^a   de Wit, Elzo ^a   de Laat, Wouter ^a   Hannon, Gregory J ^b   Clevers, Hans C ^a   Smith, Andrew D ^c   Ketting, René F ^a,d  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d Institute for Molecular Biology   (Germany)

Author keywords

Adult stem cells; Differentiation; DNA Methylation; Enhancer; Methylome; Tcf4

Indexed keywords

PROTEIN TCF4; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; CHROMATIN; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, MOUSE; TCF4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA METHYLATION; ENHANCER REGION; GENE EXPRESSION; GENE LOCUS; INTESTINE VILLUS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; SMALL INTESTINE; STEM CELL; TRANSCRIPTION INITIATION SITE; ADULT STEM CELL; ANIMAL; CHROMATIN; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS;

MAMMALIA;

ADULT STEM CELLS; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CHROMATIN; DNA METHYLATION; GENE EXPRESSION REGULATION; INTESTINE, SMALL; MICE; MOLECULAR SEQUENCE DATA; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84878248139     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-5-r50     Document Type: Article

References (47)

1. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257. 10.1016/S0092-8674(00)81656-6, 10555141.
2. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998, 19:219-220. 10.1038/890, 9662389.
3. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770. 2896277, 18600261.
4. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322. 10.1038/nature08514, 2857523, 19829295.
5. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 2008, 30:755-766. 10.1016/j.molcel.2008.05.007, 18514006.
6. Sorensen AL, Jacobsen BM, Reiner AH, Andersen IS, Collas P. Promoter DNA methylation patterns of differentiated cells are largely programmed at the progenitor stage. Mol Biol Cell 2010, 21:2066-2077. 10.1091/mbc.E10-01-0018, 2883950, 20410135.
7. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, Park J, Butler J, Rafii S, McCombie WR, Smith AD, Hannon GJ. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 2011, 44:17-28. 10.1016/j.molcel.2011.08.026, 3412369, 21924933.
8. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, Lee H, Aryee MJ, Irizarry RA, Kim K, Rossi DJ, Inlay MA, Serwold T, Karsunky H, Ho L, Daley GQ, Weissman IL, Feinberg AP. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 2010, 467:338-342. 10.1038/nature09367, 2956609, 20720541.
9. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, Berg JS, Bock C, Vasanthakumar A, Gu H, Xi Y, Liang S, Lu Y, Darlington GJ, Meissner A, Issa JP, Godley LA, Li W, Goodell MA. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 2011, 44:23-31. 10.1038/ng.1009, 3637952, 22138693.
10. Bock C, Beerman I, Lien WH, Smith ZD, Gu H, Boyle P, Gnirke A, Fuchs E, Rossi DJ, Meissner A. DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol Cell 2012, 47:633-647. 10.1016/j.molcel.2012.06.019, 22841485.
11. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007. 10.1038/nature06196, 17934449.
12. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Ann Rev Physiol 2009, 71:241-260.
13. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469:415-418. 10.1038/nature09637, 3547360, 21113151.
14. Ireland H, Houghton C, Howard L, Winton DJ. Cellular inheritance of a Cre-activated reporter gene to determine Paneth cell longevity in the murine small intestine. Dev Dyn 2005, 233:1332-1336. 10.1002/dvdy.20446, 15937933.
15. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611. 10.1038/nature07602, 19092804.
16. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, Danenberg E, van den Brink S, Korving J, Abo A, Peters PJ, Wright N, Poulsom R, Clevers H. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell stem cell 2010, 6:25-36. 10.1016/j.stem.2009.11.013, 20085740.
17. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, Toftgard R. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008, 40:1291-1299. 10.1038/ng.239, 18849992.
18. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009, 459:262-265. 10.1038/nature07935, 19329995.
19. Attwood JT, Yung RL, Richardson BC. DNA methylation and the regulation of gene transcription. Cell Mol Life Sci 2002, 59:241-257. 10.1007/s00018-002-8420-z, 11915942.
20. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009, 10:295-304.
21. van der Flier LG, van Gijn ME, Hatzis P, Kujala P, Haegebarth A, Stange DE, Begthel H, van den Born M, Guryev V, Oving I, van Es JH, Barker N, Peters PJ, van de Wetering M, Clevers H. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 2009, 136:903-912. 10.1016/j.cell.2009.01.031, 19269367.
22. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 2011, 146:1029-1041. 10.1016/j.cell.2011.08.016, 3205962, 21925323.
23. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, Antosiewicz-Bourget J, O'Malley R, Castanon R, Klugman S, Downes M, Yu R, Stewart R, Ren B, Thomson JA, Evans RM, Ecker JR. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011, 471:68-73. 10.1038/nature09798, 3100360, 21289626.
24. Schepers AG, Vries R, van den Born M, van de Wetering M, Clevers H. Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J 2011, 30:1104-1109. 10.1038/emboj.2011.26, 3061032, 21297579.
25. Heintzman ND, Ren B. Finding distal regulatory elements in the human genome. Curr Opin Genet Dev 2009, 19:541-549. 10.1016/j.gde.2009.09.006, 3321269, 19854636.
26. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, Wirbelauer C, Oakeley EJ, Gaidatzis D, Tiwari VK, Schubeler D. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011, 480:490-495.
27. Barrera LO, Li Z, Smith AD, Arden KC, Cavenee WK, Zhang MQ, Green RD, Ren B. Genome-wide mapping and analysis of active promoters in mouse embryonic stem cells and adult organs. Genome Res 2008, 18:46-59. 2134779, 18042645.
28. Wang P, Lin C, Smith ER, Guo H, Sanderson BW, Wu M, Gogol M, Alexander T, Seidel C, Wiedemann LM, Ge K, Krumlauf R, Shilatifard A. Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 2009, 29:6074-6085. 10.1128/MCB.00924-09, 2772563, 19703992.
29. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, Ren B. A map of the cis-regulatory sequences in the mouse genome. Nature 2012, 488:116-120. 10.1038/nature11243, 22763441.
30. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJ, Zhu Y, Kaaij LJ, van Ijcken W, Gribnau J, Heard E, de Laat W. The inactive × chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev 2011, 25:1371-1383. 10.1101/gad.633311, 3134081, 21690198.
31. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998, 19:379-383. 10.1038/1270, 9697701.
32. van Es JH, Haegebarth A, Kujala P, Itzkovitz S, Koo BK, Boj SF, Korving J, van den Born M, van Oudenaarden A, Robine S, Clevers H. A critical role for the Wnt effector Tcf4 in adult intestinal homeostatic self-renewal. Mol Cell Biol 2012, 32:1918-1927. 10.1128/MCB.06288-11, 3347420, 22393260.
33. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ, Winton DJ. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterol 2004, 126:1236-1246.
34. Lin H, Yamada Y, Nguyen S, Linhart H, Jackson-Grusby L, Meissner A, Meletis K, Lo G, Jaenisch R. Suppression of intestinal neoplasia by deletion of Dnmt3b. Mol Cell Biol 2006, 26:2976-2983. 10.1128/MCB.26.8.2976-2983.2006, 1446955, 16581773.
35. Linhart HG, Lin H, Yamada Y, Moran E, Steine EJ, Gokhale S, Lo G, Cantu E, Ehrich M, He T, Meissner A, Jaenisch R. Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev 2007, 21:3110-3122. 10.1101/gad.1594007, 2081977, 18056424.
36. John S, Sabo PJ, Thurman RE, Sung MH, Biddie SC, Johnson TA, Hager GL, Stamatoyannopoulos JA. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 2011, 43:264-268. 10.1038/ng.759, 21258342.
37. Samstein RM, Arvey A, Josefowicz SZ, Peng X, Reynolds A, Sandstrom R, Neph S, Sabo P, Kim JM, Liao W, Li MO, Leslie C, Stamatoyannopoulos JA, Rudensky AY. Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification. Cell 2012, 151:153-166. 10.1016/j.cell.2012.06.053, 3493256, 23021222.
38. Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T, Simmons CA, Pearce KH, Biddie SC, Sabo PJ, Thurman RE, Stamatoyannopoulos JA, Hager GL. DNA methylation status predicts cell type-specific enhancer activity. EMBO J 2011, 30:3028-3039. 10.1038/emboj.2011.210, 3160184, 21701563.
39. Chen C, Fang R, Davis C, Maravelias C, Sibley E. Pdx1 inactivation restricted to the intestinal epithelium in mice alters duodenal gene expression in enterocytes and enteroendocrine cells. Am J Physiol Gastrointest Liver Physiol 2009, 297:G1126-1137. 10.1152/ajpgi.90586.2008, 2850094, 19808654.
40. Grandori C, Cowley SM, James LP, Eisenman RN. The Myc/Max/Mad network and the transcriptional control of cell behavior. Ann Rev Cell Dev Biol 2000, 16:653-699.
41. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
42. Bamshad M, Lin RC, Law DJ, Watkins WC, Krakowiak PA, Moore ME, Franceschini P, Lala R, Holmes LB, Gebuhr TC, Bruneau BG, Schinzel A, Seidman JG, Seidman CE, Jorde LB. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet 1997, 16:311-315. 10.1038/ng0797-311, 9207801.
43. Wardle FC, Odom DT, Bell GW, Yuan B, Danford TW, Wiellette EL, Herbolsheimer E, Sive HL, Young RA, Smith JC. Zebrafish promoter microarrays identify actively transcribed embryonic genes. Genome Biol 2006, 7:R71. 10.1186/gb-2006-7-8-r71, 1779600, 16889661.
44. Simonis M, Kooren J, de Laat W. An evaluation of 3C-based methods to capture DNA interactions. Nat Methods 2007, 4:895-901. 10.1038/nmeth1114, 17971780.
45. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431. 10.1093/bioinformatics/18.11.1427, 12424112.
46. Revet I, Huizenga G, Chan A, Koster J, Volckmann R, van Sluis P, Ora I, Versteeg R, Geerts D. The MSX1 homeobox transcription factor is a downstream target of PHOX2B and activates the Delta-Notch pathway in neuroblastoma. Exp Cell Res 2008, 314:707-719. 10.1016/j.yexcr.2007.12.008, 18201699.
47. van de Werken HJ, Landan G, Holwerda SJ, Hoichman M, Klous P, Chachik R, Splinter E, Valdes-Quezada C, Oz Y, Bouwman BA, Verstegen MJ, de Wit E, Tanay A, de Laat W. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat Methods 2012, 9:969-972. 10.1038/nmeth.2173, 22961246.