Thyroid hormone receptor actions on transcription in amphibia: The roles of histone modification and chromatin disruption

Cell & Bioscience

Liezhen Fu¹  Luan Wen¹  Kenta Fujimoto²  Kazuo Matsuura¹  Yun-Bo Shi¹ 

[1] 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), Bethesda, Maryland, 20892, USA;Division of Gene Structure and Function, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, Hidaka-shi, Saitama, 350-1241, Japan

关键词: Nucleosome removal;    Histone acetylation;    Histone methylation;    Xenopus laevis and tropicalis;    Metamorphosis;    Apoptosis;    Stem cell;    Thyroid hormone receptor;    Corepressor;    Transcriptional coactivator;   

Others  :  793057
DOI  :  10.1186/2045-3701-2-42

 received in 2012-10-30, accepted in 2012-11-21,  发布年份 2012

【 摘 要 】

Thyroid hormone (T3) plays diverse roles in adult organ function and during vertebrate development. The most important stage of mammalian development affected by T3 is the perinatal period when plasma T3 level peaks. Amphibian metamorphosis resembles this mammalian postembryonic period and is absolutely dependent on T3. The ability to easily manipulate this process makes it an ideal model to study the molecular mechanisms governing T3 action during vertebrate development. T3 functions mostly by regulating gene expression through T3 receptors (TRs). Studies in vitro, in cell cultures and reconstituted frog oocyte transcription system have revealed that TRs can both activate and repress gene transcription in a T3-dependent manner and involve chromatin disruption and histone modifications. These changes are accompanied by the recruitment of diverse cofactor complexes. More recently, genetic studies in mouse and frog have provided strong evidence for a role of cofactor complexes in T3 signaling in vivo. Molecular studies on amphibian metamorphosis have also revealed that developmental gene regulation by T3 involves histone modifications and the disruption of chromatin structure at the target genes as evidenced by the loss of core histones, arguing that chromatin remodeling is an important mechanism for gene activation by liganded TR during vertebrate development.

【 授权许可】

   
2012 Shi et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Oppenheimer JH: Thyroid hormone action at the cellular level. Science 1979, 203:971-979.
• [2]Yen PM: Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001, 81:1097-1142.
• [3]Canaris GJ, Manowitz NR, Mayor G, Ridgway EC: The Colorado thyroid disease prevalence study. Arch Intern Med 2000, 160:526-534.
• [4]Franklyn JA, Gammage MD: Thyroid disease: Effects on cardiovascular function. TEM 1996, 7:50-54.
• [5]Silva JE: Thyroid hormone control of thermogenesis and energy balance. Thyroid 1995, 5:481-492.
• [6]Freake HC, Oppenheimer JH: Thermogenesis and thyroid function. Annu Rev Nutr 1995, 15:263-291.
• [7]Hetzel BS: The story of iodine deficiency: An international challenge in nutrition. Oxford: Oxford University Press; 1989.
• [8]Porterfield SP, Hendrich CE: The role of thyroid hormones in prenatal and neonatal neurological development–current perspectives. Endocr Rev 1993, 14:94-106.
• [9]Gilbert LI, Tata JR, Atkinson BG: Metamorphosis: Post-embryonic reprogramming of gene expression in amphibian and insect cells. New York: Academic Press; 1996.
• [10]Shi Y-B: Amphibian Metamorphosis: From morphology to molecular biology. New York: John Wiley & Sons, Inc.; 1999.
• [11]Gudernatch JF: Feeding experiments on tadpoles. I. The influence of specific organs given as food on growth and differentiation: a contribution to the knowledge of organs with internal secretion. Arch Entwicklungsmech Org 1912, 35:457-483.
• [12]Tata JR: Gene expression during metamorphosis: an ideal model for post-embryonic development. BioEssays 1993, 15:239-248.
• [13]Davis PJ, Davis FB: Nongenomic actions of thyroid hormone. Thyroid 1996, 6:497-504.
• [14]Shi Y-B, Wong J, Puzianowska-Kuznicka M, Stolow M: Tadpole competence and tissue-specific temporal regulation of amphibian metamorphosis: roles of thyroid hormone and its receptors. BioEssays 1996, 18:391-399.
• [15]Davis PJ, Davis FB: Nongenomic actions of thyroid hormone on the heart. Thyroid 2002, 12:459-466.
• [16]Parkison C, Ashizawa K, McPhie P, Lin KH, Cheng SY: The monomer of pyruvate kinase, subtype M1, is both a kinase and a cytosolic thyroid hormone binding protein. Biochem Biophys Res Commun 1991, 179:668-674.
• [17]Shi Y-B, Liang VC-T, Parkison C, Cheng S-Y: Tissue-dependent developmental expression of a cytosolic thyroid hormone protein gene in Xenopus: its role in the regulation of amphibian metamorphosis. FEBS Lett 1994, 355:61-64.
• [18]Bassett JH, Harvey CB, Williams GR: Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions. Mol Cell Endocrinol 2003, 213:1-11.
• [19]Davis PJ, Davis FB, Cody V: Membrane receptors mediating thyroid hormone action. Trends Endocrinol Metab 2005, 16:429-435.
• [20]Storey NM, Gentile S, Ullah H, Russo A, Muessel M, Erxleben C, Armstrong DL: Rapid signaling at the plasma membrane by a nuclear receptor for thyroid hormone. Proc Natl Acad Sci U S A 2006, 103:5197-5201.
• [21]Guigon CJ, Cheng SY: Novel non-genomic signaling of thyroid hormone receptors in thyroid carcinogenesis. Mol Cell Endocrinol 2009, 308:63-69.
• [22]Laudet V, Gronemeyer H: The nuclear receptor FactsBook. San Diego: Academic Press; 2002.
• [23]Cheng SY: Thyroid hormone receptor mutations and disease: beyond thyroid hormone resistance. Trends Endocrinol Metab 2005, 16:176-182.
• [24]Sakurai A, Takeda K, Ain K, Ceccarelli P, Nakai A, Seino S, Bell GI, Refetoff S, DeGroot LJ: Generalized resistance to thyroid hormone associated with a mutation in the ligand-binding domain of the human thyroid hormone receptor beta. Proc Natl Acad Sci U S A 1989, 86:8977-8981.
• [25]Chatterjee VKK, Nagaya T, Madison LD, Patta S, Rantoumis A, Jameson JL: Thyroid hormone resistance syndrome: Inhibition of normal receptor function by mutant thyroid hormone receptors. J Clin Invest 1991, 87:1977-1984.
• [26]Bochukova E, Schoenmakers N, Agostini M, Schoenmakers E, Rajanayagam O, Keogh JM, Henning E, Reinemund J, Gevers E, Sarri M, et al.: A mutation in the thyroid hormone receptor alpha gene. N Engl J Med 2012, 366:243-249.
• [27]van Mullem A, van Heerebeek R, Chrysis D, Visser E, Medici M, Andrikoula M, Tsatsoulis A, Peeters R, Visser TJ: Clinical phenotype and mutant TRalpha1. N Engl J Med 2012, 366:1451-1453.
• [28]Flamant F, Samarut J: Thyroid hormone receptors: Lessons from knockout and knock-in mutant mice. Trends in Endocrinology and metabolism 2003, 14:85-90.
• [29]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.
• [30]Brown DD, Cai L: Amphibian metamorphosis. Dev Biol 2007, 306:20-33.
• [31]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.
• [32]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.
• [33]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.
• [34]Shi Y-B: Dual functions of thyroid hormone receptors in vertebrate development: the roles of histone-modifying cofactor complexes. Thyroid 2009, 19:987-999.
• [35]Nakajima K, Yaoita Y: Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn 2003, 227:246-255.
• [36]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.
• [37]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.
• [38]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.
• [39]Sachs LM, Damjanovski S, Jones PL, Li Q, Amano T, Ueda S, Shi YB, Ishizuya-Oka A: Dual functions of thyroid hormone receptors during Xenopus development. Comp Biochem Physiol B Biochem Mol Biol 2000, 126:199-211.
• [40]Shi Y-B: Molecular biology of amphibian metamorphosis: A new approach to an old problem. Trends Endocrinol Metab 1994, 5:14-20.
• [41]Lazar MA: Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 1993, 14:184-193.
• [42]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.
• [43]Tsai MJ, O'Malley BW: Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Ann Rev Biochem 1994, 63:451-486.
• [44]Wong J, Shi YB, Wolffe AP: A role for nucleosome assembly in both silencing and activation of the Xenopus TR beta A gene by the thyroid hormone receptor. Genes Dev 1995, 9:2696-2711.
• [45]Wong J, Shi Y-B, Wolffe AP: Determinants of chromatin disruption and transcriptional regulation instigated by the thyroid hormone receptor: hormone-regulated chromatin disruption is not sufficient for transcriptinal activation. EMBO J 1997, 16:3158-3171.
• [46]Wong J, Patterton D, Imhof D, Guschin D, Shi Y-B, Wolffe AP: Distinct requirements for chromatin assembly in transcriptional repression by thyroid hormone receptor and histone deacetylase. EMBO J 1998, 17:520-534.
• [47]McKenna NJ, O'Malley BW: Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 2002, 108:465-474.
• [48]Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK, et al.: Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 1995, 377:397-404.
• [49]Chen JD, Evans RM: A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 1995, 377:454-457.
• [50]Burke LJ, Baniahmad A: Co-repressors 2000. FASEB J 2000, 14:1876-1888.
• [51]Jones PL, Shi Y-B: N-CoR-HDAC corepressor complexes: Roles in transcriptional regulation by nuclear hormone receptors. In Current Topics in Microbiology and Immunology: Protein Complexes that Modify Chromatin. 274th edition. Edited by Workman JL. Berlin: Springer-Verlag; 2003:237-268.
• [52]Glass CK, Rosenfeld MG: The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 2000, 14:121-141.
• [53]Ito M, Roeder RG: The TRAP/SMCC/Mediator complex and thyroid hormone receptor function. Trends Endocrinol Metab 2001, 12:127-134.
• [54]Zhang J, Lazar MA: The mechanism of action of thyroid hormones. Annu Rev Physiol 2000, 62:439-466.
• [55]Huang Z-Q, Li J, Sachs LM, Cole PA, Wong J: A role for cofactor–cofactor and cofactor–histone interactions in targeting p300, SWI/SNF and Mediator for transcription. EMBO J 2003, 22:2146-2155.
• [56]McKenna NJ, O'Malley BW: Nuclear receptors, coregulators, ligands, and selective receptor modulators: making sense of the patchwork quilt. Ann N Y Acad Sci 2001, 949:3-5.
• [57]Rachez C, Freedman LP: Mediator complexes and transcription. Curr Opin Cell Biol 2001, 13:274-280.
• [58]Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM: Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 1997, 90:569-580.
• [59]Demarest SJ, Martinez-Yamout M, Chung J, Chen H, Xu W, Dyson HJ, Evans RM, Wright PE: Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 2002, 415:549-553.
• [60]Onate SA, Tsai SY, Tsai MJ, O'Malley BW: Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 1995, 270:1354-1357.
• [61]Meng X, Yang YF, Cao X, Govindan MV, Shuen M, Hollenberg AN, Mymryk JS, Walfish PG: Cellular context of coregulator and adaptor proteins regulates human adenovirus 5 early region 1A-dependent gene activation by the thyroid hormone receptor. Mol Endocrinol 2003, 17:1095-1105.
• [62]Wahlstrom GM, Vennstrom B, Bolin MB: The adenovirus E1A protein is a potent coactivator for thyroid hormone receptors. Mol Endocrinol 1999, 13:1119-1129.
• [63]Sato Y, Ding A, Heimeier RA, Yousef AF, Mymryk JS, Walfish PG, Shi Y-B: The adenoviral E1A protein displaces corepressors and relieves gene repression by unliganded thyroid hormone receptors in vivo. Cell Res 2009, 19:783-792.
• [64]Perissi V, Jepsen K, Glass CK, Rosenfeld MG: Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet 2010, 11:109-123.
• [65]O'Malley BW, Malovannaya A, Qin J: Minireview: nuclear receptor and coregulator proteomics–2012 and beyond. Mol Endocrinol 2012, 26:1646-1650.
• [66]Bulynko YA, O'Malley BW: Nuclear receptor coactivators: structural and functional biochemistry. Biochemistry 2011, 50:313-328.
• [67]McKenna NJ, Cooney AJ, DeMayo FJ, Downes M, Glass CK, Lanz RB, Lazar MA, Mangelsdorf DJ, Moore DD, Qin J, et al.: Minireview: Evolution of NURSA, the Nuclear Receptor Signaling Atlas. Mol Endocrinol 2009, 23:740-746.
• [68]Yoon H-G, Chan DW, Huang ZQ, Li J, Fondell JD, Qin J, Wong J: Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. EMBO J 2003, 22:1336-1346.
• [69]Zhang J, Kalkum M, Chait BT, Roeder RG: The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell 2002, 9:611-623.
• [70]Ishizuka T, Lazar MA: The N-CoR/histone deacetylase 3 complex is required for repression by thyroid hormone receptor. Mol Cell Biol 2003, 23:5122-5131.
• [71]Guenther MG, Lane WS, Fischle W, Verdin E, Lazar MA, Shiekhattar R: A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes & Devel 2000, 14:1048-1057.
• [72]Li J, Wang J, Wang J, Nawaz Z, Liu JM, Qin J, Wong J: Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J 2000, 19:4342-4350.
• [73]Stewart D, Tomita A, Shi YB, Wong J: Chromatin immunoprecipitation for studying transcriptional regulation in Xenopus oocytes and tadpoles. Methods Mol Biol 2006, 322:165-181.
• [74]Stewart MD, Li J, Wong J: Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol 2005, 25:2525-2538.
• [75]Li J, Lin Q, Yoon HG, Huang ZQ, Strahl BD, Allis CD, Wong J: Involvement of histone methylation and phosphorylation in regulation of transcription by thyroid hormone receptor. Mol Cell Biol 2002, 22:5688-5697.
• [76]Jones PL, Sachs LM, Rouse N, Wade PA, Shi YB: Multiple N-CoR complexes contain distinct histone deacetylases. J Biol Chem 2001, 276:8807-8811.
• [77]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.
• [78]Heimeier RA, Hsia VS-C, Shi Y-B: Participation of BAF57 and BRG1-Containing Chromatin Remodeling Complexes in Thyroid Hormone-Dependent Gene Activation during Vertebrate Development. Mol Endocrinol 2008, 22:1065-1077.
• [79]Sheppard HM, Harries JC, Hussain S, Bevan C, Heery DM: Analysis of the steroid receptor coactivator 1 (SRC1)-CREB binding protein interaction interface and its importance for the function of SRC1. Mol Cell Biol 2001, 21:39-50.
• [80]Li J, O'Malley BW, Wong J: p300 requires its histone acetyltransferase activity and SRC-1 interaction domain to facilitate thyroid hormone receptor activation in chromatin. Mol And Cell Biol 2000, 20:2031-2042.
• [81]Torchia J, Rose DW, Inostroza J, Kamei Y, Westin S, Glass CK, Rosenfeld MG: The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 1997, 387:677-684.
• [82]Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, Aswad DW, Stallcup MR: Regulation of transcription by a protein methyltransferase. Science 1999, 284:2174-2177.
• [83]Koh SS, Chen DG, Lee YH, Stallcup MR: Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J Biol Chem 2001, 276:1089-1098.
• [84]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.
• [85]Matsuda H, Paul BD, Choi CY, Shi Y-B: Contrasting effects of two alternative splicing forms of coactivator-associated arginine methyltransferase 1 on thyroid hormone receptor-mediated transcription in Xenopus laevis. Mol Endocrinology 2007, 21:1082-1094.
• [86]Havis E, Sachs LM, Demeneix BA: Metamorphic T3-response genes have specific co-regulator requirements. EMBO Reports 2003, 4:883-888.
• [87]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.
• [88]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.
• [89]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.
• [90]Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O'Malley BW: The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is requried for normal growth, puberty, female reproductive function, and mammary gland development. Proc Nat Acad Sci USA 2000, 97:6379-6384.
• [91]Gehin M, Mark M, Dennefeld C, Dierich A, Gronemeyer H, Chambon P: The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol Cell Biol 2002, 22:5923-5927.
• [92]Yao TP, Oh SP, Fuchs M, Zhou ND, Ch'ng LE, Newsome D, Bronson RT, Li E, Livingston DM, Eckner R: Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998, 93:361-372.
• [93]Wang Z, Rose DW, Hermanson O, Liu F, Herman T, Wu W, Szeto D, Gleiberman A, Krones A, Pratt K, et al.: Regulation of somatic growth by the p160 coactivator p/CIP. Proc Nat Acad Sci USA 2000, 97:13549-13554.
• [94]Jepsen K, Hermanson O, Onami TM, Gleiberman AS, Lunyak V, McEvilly RJ, Kurokawa R, Kumar V, Liu F, Seto E, et al.: Combinatorial roles of the nuclear receptor corepressor in transcription and development [In Process Citation]. Cell 2000, 102:753-763.
• [95]Ito M, Yuan CX, Okano HJ, Darnell RB, Roeder RG: Involvement of the TRAP220 component of the TRAP/SMCC coactivator complex in embryonic development and thyroid hormone action. Mol Cell 2000, 5:683-693.
• [96]Weiss RE, Xu J, Ning G, Pohlenz J, O’Malley BW, Refetoff S: Mice deficient in the steroid receptor co-activator 1 (SRC-1) are resistant to thyroid hormone. EMBO J 1999, 18:1900-1904.
• [97]Astapova I, Lee LJ, Morales C, Tauber S, Bilban M, Hollenberg AN: The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc Natl Acad Sci 2008, 105:19544-19549.
• [98]You SH, Liao X, Weiss RE, Lazar MA: The interaction between nuclear receptor corepressor and histone deacetylase 3 regulates both positive and negative thyroid hormone action in vivo. Mol Endocrinol 2010, 24:1359-1367.
• [99]Pei L, Leblanc M, Barish G, Atkins A, Nofsinger R, Whyte J, Gold D, He M, Kawamura K, Li HR, et al.: Thyroid hormone receptor repression is linked to type I pneumocyte-associated respiratory distress syndrome. Nat Med 2011, 17:1466-1472.
• [100]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.
• [101]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.
• [102]Paul BD, Shi Y-B: Distinct expression profiles of transcriptional coactivators for thyroid hormone receptors during Xenopus laevis metamorphosis. Cell Research 2003, 13:459-464.
• [103]Perlman AJ, Stanley F, Samuels HH: Thyroid hormone nuclear receptor. Evidence for multimeric organization in chromatin. J Biol Chem 1982, 257:930-938.
• [104]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.
• [105]Hsia VS-C, Shi Y-B: Chromatin Disruption and Histone Acetylation in the Regulation of HIV-LTR by Thyroid Hormone Receptor. Mol Cell Biol 2002, 22:4043-4052.
• [106]Amaya E, Offield MF, Grainger RM: Frog genetics: Xenopus tropicalis jumps into the future. Trends Genet 1998, 14:253-255.
• [107]Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, et al.: The genome of the Western clawed frog Xenopus tropicalis. Science 2010, 328:633-636.
• [108]McAvoy JW, Dixon KE: Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis. J Exp Zool 1977, 202:129-138.
• [109]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
• [110]Shi Y-B, Ishizuya-Oka A: Biphasic intestinal development in amphibians: Embryogensis and remodeling during metamorphosis. Current Topics in Develop Biol 1996, 32:205-235.
• [111]Ishizuya-Oka A, Shi YB: Evolutionary insights into postembryonic development of adult intestinal stem cells. Cell Biosci 2011, 1:37. BioMed Central Full Text
• [112]Sun G, Shi Y-B: Thyroid hormone regulation of adult intestinal stem cell development: Mechanisms and evolutionary conservations. Int J Biol Sci 2012, 8:1217-1224.
• [113]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.
• [114]Li J, Lin Q, Wang W, Wade P, Wong J: Specific targeting and constitutive association of histone deacetylase complexes during transcriptional repression. Genes Dev 2002, 16:687-692.
• [115]Sharma D, Fondell JD: Ordered recruitment of histone acetyltransferases and the TRAP/Mediator complex to thyroid hormone-responsive promoters in vivo. Proc Natl Acad Sci U S A 2002, 99:7934-7939.
• [116]Liu Y, Xia X, Fondell JD, Yen PM: Thyroid hormone-regulated target genes have distinct patterns of coactivator recruitment and histone acetylation. Mol Endocrinol 2006, 20:483-490.
• [117]Sachs LM, Shi Y-B: Targeted chromatin binding and histone acetylation in vivo by thyroid hormone receptor during amphibian development. PNAS 2000, 97:13138-13143.
• [118]Sachs LM, Amano T, Shi YB: An essential role of histone deacetylases in postembryonic organ transformations in Xenopus laevis. Int J Mol Med 2001, 8:595-601.
• [119]Sachs LM, Amano T, Rouse N, Shi YB: Involvement of histone deacetylase at two distinct steps in gene regulation during intestinal development in Xenopus laevis. Dev Dyn 2001, 222:280-291.
• [120]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.
• [121]Grimaldi A, Buisine N, Miller T, Shi YB, Sachs LM: Mechanisms of thyroid hormone receptor action during development: Lessons from amphibian studies. Biochim Biophys Acta 2012. In press
• [122]Matsuura K, Fujimoto K, Das B, Fu L, Lu CD, Shi YB: Histone H3K79 methyltransferase Dot1L is directly activated by thyroid hormone receptor during Xenopus metamorphosis. Cell Biosci 2012, 2:25. BioMed Central Full Text
• [123]Fujimoto K, Matsuura K, Hu-Wang E, Lu R, Shi YB: Thyroid Hormone Activates Protein Arginine Methyltransferase 1 Expression by Directly Inducing c-Myc Transcription during Xenopus Intestinal Stem Cell Development. J Biol Chem 2012, 287:10039-10050.
• [124]Matsuda H, Shi YB: An essential and evolutionarily conserved role of protein arginine methyltransferase 1 for adult intestinal stem cells during postembryonic development. Stem Cells 2010, 28:2073-2083.
• [125]Young JJ, Cherone JM, Doyon Y, Ankoudinova I, Faraji FM, Lee AH, Ngo C, Guschin DY, Paschon DE, Miller JC, et al.: Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proc Natl Acad Sci U S A 2011, 108:7052-7057.
• [126]Lei Y, Guo X, Liu Y, Cao Y, Deng Y, Chen X, Cheng CH, Dawid IB, Chen Y, Zhao H: Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci U S A 2012, 109:17484-17489.
• [127]Hsia VS-C, Wang H, Shi Y-B: Involvement of Chromatin and Histone Acetylation in the Regulation of HIV-LTR by Thyroid Hormone Receptor. Cell Research 2001, 11:8-16.