Histone H3K79 methyltransferase Dot1L is directly activated by thyroid hormone receptor during Xenopus metamorphosis

Cell & Bioscience

Yun-Bo Shi²  Christopher D Lu²  Liezhen Fu²  Biswajit Das³  Kenta Fujimoto¹  Kazuo Matsuura² 

[1] Present address: Division of Gene Structure and Function, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, Hidaka-shi, Saitama, 350-1241, Japan;Section on Molecular Morphogenesis, Program in Cellular Regulation and Metabolism (PCRM), Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), 18 Library Dr, Bethesda, MD, 20892, USA;Present address: Laboratory of Immunopathogenesis and Bioinformatics, Clinical Services Program, SAIC-Frederick, Inc, Frederick National Laboratory for Cancer Research, Frederick, MD, 21702, USA

关键词: Histone methylation;    Xenopus laevis and tropicalis;    Metamorphosis;    Thyroid hormone receptor;    Intestinal stem cell development;    Dot1L;   

Others  :  799004
DOI  :  10.1186/2045-3701-2-25

 received in 2012-05-08, accepted in 2012-07-16,  发布年份 2012

【 摘 要 】

Background

Thyroid hormone (T3) is important for adult organ function and vertebrate development. Amphibian metamorphosis is totally dependent on T3 and offers a unique opportunity to study how T3 controls postembryonic development in vertebrates. Earlier studies have demonstrated that TR mediates the metamorphic effects of T3 in Xenopus laevis. Liganded TR recruits histone modifying coactivator complexes to target genes during metamorphosis. This leads to nucleosomal removal and histone modifications, including methylation of histone H3 lysine (K) 79, in the promoter regions, and the activation of T3-inducible genes.

Results

We show that Dot1L, the only histone methyltransferase capable of methylating H3K79, is directly regulated by TR via binding to a T3 response element in the promoter region during metamorphosis in Xenopus tropicalis, a highly related species of Xenopus laevis. We further show that Dot1L expression in both the intestine and tail correlates with the transformation of the organs.

Conclusions

Our findings suggest that TR activates Dot1L, which in turn participates in metamorphosis through a positive feedback to enhance H3K79 methylation and gene activation by liganded TR.

【 授权许可】

   
2012 Matsuura et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Tata JR: Gene expression during metamorphosis: an ideal model for post-embryonic development. BioEssays 1993, 15:239-248.
• [2]Yen PM: Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001, 81:1097-1142.
• [3]Hetzel BS: The story of iodine deficiency: An international challenge in nutrition. Oxford University Press, Oxford; 1989.
• [4]Gilbert LI, Tata JR, Atkinson BG: Metamorphosis: Post-embryonic reprogramming of gene expression in amphibian and insect cells. Academic, New York; 1996.
• [5]Shi Y-B: Amphibian Metamorphosis: From morphology to molecular biology. Wiley, New York; 1999.
• [6]Shi YB, Hasebe T, Fu L, Fujimoto K, Ishizuya-Oka A: The development of the adult intestinal stem cells: Insights from studies on thyroid hormone-dependent amphibian metamorphosis. Cell Biosci 2011, 1:30. BioMed Central Full Text
• [7]Ishizuya-Oka A, Shi YB: Evolutionary insights into postembryonic development of adult intestinal stem cells. Cell Biosci 2011, 1:37. BioMed Central Full Text
• [8]Lazar MA: Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 1993, 14:184-193.
• [9]Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P: The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
• [10]Tsai MJ, O’Malley BW: Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Ann Rev Biochem 1994, 63:451-486.
• [11]Schreiber AM, Das B, Huang H, Marsh-Armstrong N, Brown DD: Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. PNAS 2001, 98:10739-10744.
• [12]Brown DD, Cai L: Amphibian metamorphosis. Dev Biol 2007, 306:20-33.
• [13]Buchholz DR, Hsia VS-C, Fu L, Shi Y-B: A dominant negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Mol Cell Biol 2003, 23:6750-6758.
• [14]Buchholz DR, Tomita A, Fu L, Paul BD, Shi Y-B: Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Mol Cell Biol 2004, 24:9026-9037.
• [15]Buchholz DR, Paul BD, Fu L, Shi YB: Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol 2006, 145:1-19.
• [16]Shi Y-B: Dual functions of thyroid hormone receptors in vertebrate development: the roles of histone-modifying cofactor complexes. Thyroid 2009, 19:987-999.
• [17]Nakajima K, Yaoita Y: Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn 2003, 227:246-255.
• [18]Denver RJ, Hu F, Scanlan TS, Furlow JD: Thyroid hormone receptor subtype specificity for hormone-dependent neurogenesis in Xenopus laevis. Dev Biol 2009, 326:155-168.
• [19]Bagamasbad P, Howdeshell KL, Sachs LM, Demeneix BA, Denver RJ: A role for basic transcription element-binding protein 1 (BTEB1) in the autoinduction of thyroid hormone receptor beta. J Biol Chem 2008, 283:2275-2285.
• [20]Schreiber AM, Mukhi S, Brown DD: Cell-cell interactions during remodeling of the intestine at metamorphosis in Xenopus laevis. Dev Biol 2009, 331:89-98.
• [21]Bilesimo P, Jolivet P, Alfama G, Buisine N, Le Mevel S, Havis E, Demeneix BA, Sachs LM: Specific Histone Lysine 4 Methylation Patterns Define TR-Binding Capacity and Differentiate Direct T3 Responses. Mol Endocrinol 2011, 25:225-237.
• [22]Matsuura K, Fujimoto K, Fu L, Shi Y-B: Liganded thyroid hormone receptor induces nucleosome removal and histone modifications to activate transcription during larval intestinal cell death and adult stem cell development. Endocrinology 2012, 153:961-972.
• [23]Wang X, Matsuda H, Shi Y-B: Developmental regulation and function of thyroid hormone receptors and 9-cis retinoic acid receptors during Xenopus tropicalis metamorphosis. Endocrinology 2008, 149:5610-5618.
• [24]Tomita A, Buchholz DR, Shi Y-B: Recruitment of N-CoR/SMRT-TBLR1 corepressor complex by unliganded thyroid hormone receptor for gene repression during frog development. Mol Cell Biol 2004, 24:3337-3346.
• [25]Sachs LM, Jones PL, Havis E, Rouse N, Demeneix BA, Shi Y-B: N-CoR recruitment by unliganded thyroid hormone receptor in gene repression during Xenopus laevis development. Mol Cell Biol 2002, 22:8527-8538.
• [26]Sato Y, Buchholz DR, Paul BD, Shi Y-B: A role of unliganded thyroid hormone receptor in postembryonic development in Xenopus laevis. Mech Dev 2007, 124:476-488.
• [27]Matsuda H, Paul BD, Choi CY, Hasebe T, Shi Y-B: Novel functions of protein arginine methyltransferase 1 in thyroid hormone receptor-mediated transcription and in the regulation of metamorphic rate in Xenopus laevis. Mol Cell Biol 2009, 29:745-757.
• [28]Paul BD, Buchholz DR, Fu L, Shi Y-B: Tissue- and gene-specific recruitment of steroid receptor coactivator-3 by thyroid hormone receptor during development. J Biol Chem 2005, 280:27165-27172.
• [29]Paul BD, Fu L, Buchholz DR, Shi Y-B: Coactivator recruitment is essential for liganded thyroid hormone receptor to initiate amphibian metamorphosis. Mol Cell Biol 2005, 25:5712-5724.
• [30]Paul BD, Buchholz DR, Fu L, Shi Y-B: SRC-p300 coactivator complex is required for thyroid hormone induced amphibian metamorphosis. J Biol Chem 2007, 282:7472-7481.
• [31]Havis E, Sachs LM, Demeneix BA: Metamorphic T3-response genes have specific co-regulator requirements. EMBO Reports 2003, 4:883-888.
• [32]Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE: Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 1998, 150:613-632.
• [33]Nguyen AT, Zhang Y: The diverse functions of Dot1 and H3K79 methylation. Genes Dev 2011, 25:1345-1358.
• [34]Greer EL, Shi Y: Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 2012, 13:343-357.
• [35]Dillon SC, Zhang X, Trievel RC, Cheng X: The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 2005, 6:227. BioMed Central Full Text
• [36]Barry ER, Corry GN, Rasmussen TP: Targeting DOT1L action and interactions in leukemia: the role of DOT1L in transformation and development. Expert Opin Ther Targets 2010, 14:405-418.
• [37]Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y: Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 2002, 12:1052-1058.
• [38]Jones B, Su H, Bhat A, Lei H, Bajko J, Hevi S, Baltus GA, Kadam S, Zhai H, Valdez R, et al.: The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 2008, 4:e1000190.
• [39]Kouzarides T: Chromatin modifications and their function. Cell 2007, 128:693-705.
• [40]Shilatifard A: Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 2006, 75:243-269.
• [41]Wang Z, Schones DE, Zhao K: Characterization of human epigenomes. Curr Opin Genet Dev 2009, 19:127-134.
• [42]Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y: Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
• [43]Cao R, Zhang Y: The functions of E(Z)/EZH2- mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004, 14:155-164.
• [44]Li B, Carey M, Workman JL: The role of chromatin during transcription. Cell 2007, 128:707-719.
• [45]Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K: Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40:897-903.
• [46]Roh TY, Cuddapah S, Cui K, Zhao K: The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 2006, 103:15782-15787.
• [47]Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K: High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837.
• [48]Maunakea AK, Chepelev I, Zhao K: Epigenome mapping in normal and disease States. Circ Res 2010, 107:327-339.
• [49]Barth TK, Imhof A: Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem Sci 2010, 35:618-626.
• [50]Zhang W, Hayashizaki Y, Kone BC: Structure and regulation of the mDot1 gene, a mouse histone H3 methyltransferase. Biochem J 2004, 377:641-651.
• [51]Shi Y-B, Yaoita Y, Brown DD: Genomic organization and alternative promoter usage of the two thyroid hormone receptor ß genes in Xenopus laevis. J Biol Chem 1992, 267:733-788.
• [52]Ranjan M, Wong J, Shi YB: Transcriptional repression of Xenopus TR beta gene is mediated by a thyroid hormone response element located near the start site. J Biol Chem 1994, 269:24699-24705.
• [53]Wong J, Liang VC, Sachs LM, Shi YB: Transcription from the thyroid hormone-dependent promoter of the Xenopus laevis thyroid hormone receptor betaA gene requires a novel upstream element and the initiator, but not a TATA Box. J Biol Chem 1998, 273:14186-14193.
• [54]Wong J, Shi Y-B: Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J Biol Chem 1995, 270:18479-18483.
• [55]Buchholz DR, Ishizuya-Oka A, Shi YB: Spatial and temporal expression pattern of a novel gene in the frog Xenopus laevis: correlations with adult intestinal epithelial differentiation during metamorphosis. Gene Expr Patterns 2004, 4:321-328.
• [56]Nieuwkoop PD, Faber J: Normal table of Xenopus laevis. North Holland Publishing, Amsterdam; 1965.
• [57]Das B, Heimeier RA, Buchholz DR, Shi YB: Identification of direct thyroid hormone response genes reveals the earliest gene regulation programs during frog metamorphosis. J Biol Chem 2009, 284:34167-34178.
• [58]Sandelin A, Wasserman WW: Prediction of nuclear hormone receptor response elements. Mol Endocrinol 2005, 19:595-606.