64
Views
30
CrossRef citations to date
0
Altmetric
Article

DOT1L-Mediated H3K79 Methylation in Chromatin Is Dispensable for Wnt Pathway-Specific and Other Intestinal Epithelial Functions

, , , , &
Pages 1735-1745 | Received 28 Oct 2012, Accepted 12 Feb 2013, Published online: 20 Mar 2023

REFERENCES

  • Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403:41–45.
  • Kouzarides T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:198–209.
  • Vakoc CR, Sachdeva MM, Wang H, Blobel GA. 2006. Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol. 26:9185–9195.
  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823–837.
  • Ng HH, Ciccone DN, Morshead KB, Oettinger MA, Struhl K. 2003. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc. Natl. Acad. Sci. U. S. A. 100:1820–1825.
  • Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M. 2004. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18:1263–1271.
  • Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527.
  • Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, Vakoc AL, Kim JE, Chen J, Lazar MA, Blobel GA, Vakoc CR. 2008. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 28:2825–2839.
  • Nguyen AT, Zhang Y. 2011. The diverse functions of Dot1 and H3K79 methylation. Genes Dev. 25:1345–1358.
  • Okada Y, Feng Q, Lin Y, Jiang Q, Li Y, Coffield VM, Su L, Xu G, Zhang Y. 2005. hDOT1L links histone methylation to leukemogenesis. Cell 121:167–178.
  • Krivtsov AV, Feng Z, Lemieux ME, Faber J, Vempati S, Sinha AU, Xia X, Jesneck J, Bracken AP, Silverman LB, Kutok JL, Kung AL, Armstrong SA. 2008. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 14:355–368.
  • Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y. 2002. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12:1052–1058.
  • van Leeuwen F, Gafken PR, Gottschling DE. 2002. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109:745–756.
  • Shanower GA, Muller M, Blanton JL, Honti V, Gyurkovics H, Schedl P. 2005. Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 169:173–184.
  • Jones B, Su H, Bhat A, Lei H, Bajko J, Hevi S, Baltus GA, Kadam S, Zhai H, Valdez R, Gonzalo S, Zhang Y, Li E, Chen T. 2008. The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet. 4:e1000190. doi:10.1371/journal.pgen.1000190.
  • Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, Struhl K. 2002. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 16:1518–1527.
  • Huyen Y, Zgheib O, Ditullio RAJr, Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406–411.
  • Nguyen AT, Xiao B, Neppl RL, Kallin EM, Li J, Chen T, Wang DZ, Xiao X, Zhang Y. 2011. DOT1L regulates dystrophin expression and is critical for cardiac function. Genes Dev. 25:263–274.
  • Clevers H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469–480.
  • Pinto D, Gregorieff A, Begthel H, Clevers H. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 17:1709–1713.
  • Kuhnert F, Davis CR, Wang HT, Chu P, Lee M, Yuan J, Nusse R, Kuo CJ. 2004. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. U. S. A. 101:266–271.
  • Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, Simon-Assmann P, Clevers H, Nathke IS, Clarke AR, Winton DJ. 2004. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 18:1385–1390.
  • Sangiorgi E, Capecchi MR. 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40:915–920.
  • Takeda N, Jain R, LeBoeuf MR, Wang Q, Lu MM, Epstein JA. 2011. Interconversion between intestinal stem cell populations in distinct niches. Science 334:1420–1424.
  • Tian H, Biehs B, Warming S, Leong KG, Rangell L, Klein OD, de Sauvage FJ. 2011. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478:255–259.
  • 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. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003–1007.
  • 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. 2009. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457:608–611.
  • 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. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262–265.
  • Mahmoudi T, Boj SF, Hatzis P, Li VS, Taouatas N, Vries RG, Teunissen H, Begthel H, Korving J, Mohammed S, Heck AJ, Clevers H. 2010. The leukemia-associated Mllt10/Af10-Dot1l are Tcf4/beta-catenin coactivators essential for intestinal homeostasis. PLoS Biol. 8:e1000539. doi:10.1371/journal.pbio.1000539.
  • Mohan M, Herz HM, Takahashi YH, Lin C, Lai KC, Zhang Y, Washburn MP, Florens L, Shilatifard A. 2010. Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev. 24:574–589.
  • Castano Betancourt MC, Cailotto F, Kerkhof HJ, Cornelis FM, Doherty SA, Hart DJ, Hofman A, Luyten FP, Maciewicz RA, Mangino M, Metrustry S, Muir K, Peters MJ, Rivadeneira F, Wheeler M, Zhang W, Arden N, Spector TD, Uitterlinden AG, Doherty M, Lories RJ, Valdes AM, van Meurs JB. 2012. Genome-wide association and functional studies identify the DOT1L gene to be involved in cartilage thickness and hip osteoarthritis. Proc. Natl. Acad. Sci. U. S. A. 109:8218–8223.
  • Krivtsov AV, Armstrong SA. 2007. MLL translocations, histone modifications and leukaemia stem-cell development. Nat. Rev. Cancer 7:823–833.
  • Muntean AG, Hess JL. 2012. The pathogenesis of mixed-lineage leukemia. Annu. Rev. Pathol. 7:283–301.
  • Bitoun E, Oliver PL, Davies KE. 2007. The mixed-lineage leukemia fusion partner AF4 stimulates RNA polymerase II transcriptional elongation and mediates coordinated chromatin remodeling. Hum. Mol. Genet. 16:92–106.
  • Mueller D, Bach C, Zeisig D, Garcia-Cuellar MP, Monroe S, Sreekumar A, Zhou R, Nesvizhskii A, Chinnaiyan A, Hess JL, Slany RK. 2007. A role for the MLL fusion partner ENL in transcriptional elongation and chromatin modification. Blood 110:4445–4454.
  • Bernt KM, Zhu N, Sinha AU, Vempati S, Faber J, Krivtsov AV, Feng Z, Punt N, Daigle A, Bullinger L, Pollock RM, Richon VM, Kung AL, Armstrong SA. 2011. MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 20:66–78.
  • Jo SY, Granowicz EM, Maillard I, Thomas D, Hess JL. 2011. Requirement for Dot1l in murine postnatal hematopoiesis and leukemogenesis by MLL translocation. Blood 117:4759–4768.
  • Nguyen AT, Taranova O, He J, Zhang Y. 2011. DOT1L, the H3K79 methyltransferase, is required for MLL-AF9-mediated leukemogenesis. Blood 117:6912–6922.
  • Daigle SR, Olhava EJ, Therkelsen CA, Majer CR, Sneeringer CJ, Song J, Johnston LD, Scott MP, Smith JJ, Xiao Y, Jin L, Kuntz KW, Chesworth R, Moyer MP, Bernt KM, Tseng JC, Kung AL, Armstrong SA, Copeland RA, Richon VM, Pollock RM. 2011. Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20:53–65.
  • Nguyen AT, He J, Taranova O, Zhang Y. 2011. Essential role of DOT1L in maintaining normal adult hematopoiesis. Cell Res. 21:1370–1373.
  • Weiser MM. 1973. Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J. Biol. Chem. 248:2536–2541.
  • Verzi MP, Shin H, Ho LL, Liu XS, Shivdasani RA. 2011. Essential and redundant functions of caudal family proteins in activating adult intestinal genes. Mol. Cell. Biol. 31:2026–2039.
  • Shechter D, Dormann HL, Allis CD, Hake SB. 2007. Extraction, purification and analysis of histones. Nat. Protoc. 2:1445–1457.
  • Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. 2006. GenePattern 2.0. Nat. Genet. 38:500–501.
  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7:562–578.
  • el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, Louvard D, Chambon P, Metzger D, Robine S. 2004. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39:186–193.
  • Bjerknes M, Cheng H. 2006. Intestinal epithelial stem cells and progenitors. Methods Enzymol. 419:337–383.
  • Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY. 2001. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294:2155–2158.
  • Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, Haug J, Johnston M, Jaspersen SL, Kobor MS, Shilatifard A. 2009. Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol. Cell 35:626–641.
  • Munoz J, Stange DE, Schepers AG, van de Wetering M, Koo BK, Itzkovitz S, Volckmann R, Kung KS, Koster J, Radulescu S, Myant K, Versteeg R, Sansom OJ, van Es JH, Barker N, van Oudenaarden A, Mohammed S, Heck AJ, Clevers H. 2012. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4′ cell markers. EMBO J. 31:3079–3091.
  • Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H. 2002. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111:251–263.
  • van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, Tjon-Pon-Fong M, Moerer P, van den Born M, Soete G, Pals S, Eilers M, Medema R, Clevers H. 2002. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111:241–250.
  • Kim TH, Escudero S, Shivdasani RA. 2012. Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells. Proc. Natl. Acad. Sci. U. S. A. 109:3932–3937.
  • Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1:4. doi:10.1186/1471-213X-1-4.
  • Henikoff S, Shilatifard A. 2011. Histone modification: cause or cog? Trends Genet. 27:389–396.
  • Li Z, Nie F, Wang S, Li L. 2011. Histone H4 Lys 20 monomethylation by histone methylase SET8 mediates Wnt target gene activation. Proc. Natl. Acad. Sci. U. S. A. 108:3116–3123.
  • Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, Bernt KM, Cahan P, Marcarci BO, Unternaehrer J, Gupta PB, Lander ES, Armstrong SA, Daley GQ. 2012. Chromatin-modifying enzymes as modulators of reprogramming. Nature 483:598–602.
  • 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. 2009. 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. 29:6074–6085.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.