Direct activation of amidohydrolase domain-containing 1 gene by thyroid hormone implicates a role in the formation of adult intestinal stem cells during Xenopus metamorphosis

Endocrinology (United States)

Volumn 156, Issue 9, 2015, Pages 3381-3393

  Okada, Morihiro ^a   Miller, Thomas C ^a   Fu, Liezhen ^a   Shi, Yun Bo ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; AMIDOHYDROLASE DOMAIN CONTAINING 1; HISTIDINE AMMONIALYASE; LIOTHYRONINE RECEPTOR; THYROID HORMONE; UNCLASSIFIED DRUG; AMDHD1 PROTEIN, XENOPUS; LIOTHYRONINE; RETINOID X RECEPTOR; XENOPUS PROTEIN;

ADULT; ADULT STEM CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; EPITHELIUM CELL; GENE; GENE EXPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; INTESTINAL STEM CELL; INTESTINAL TISSUE; LARVAL STAGE; METAMORPHOSIS; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE SPECIFICITY; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; CYTOLOGY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTESTINE; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ADULT STEM CELLS; AMIDOHYDROLASES; AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTESTINES; METAMORPHOSIS, BIOLOGICAL; MICE; MOLECULAR SEQUENCE DATA; RESPONSE ELEMENTS; RETINOID X RECEPTORS; TRIIODOTHYRONINE; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84942805011     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1190     Document Type: Article

References (91)

1. MacDonald WC, Trier JS, Everett NB Cell proliferation and migration in the stomach, duodenum, and rectum of man: radioautographic studies. Gastroenterology. 1964; 46:405-417.
2. Toner PG, Carr KE, Wyburn GM The Digestive System: An Ultrastructural Atlas and Review. London, UK: Butterworth; 1971.
3. 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.
4. Shi YB, Ishizuya-Oka A. Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Curr Top Dev Biol. 1996; 32:205-235.
5. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009; 71:241-260.
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.
7. Ishizuya-Oka A., Shi YB Evolutionary insights into postembryonic development of adult intestinal stem cells. Cell Biosci. 2011; 1:37.
8. Cheng H, Leblond CP Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat. 1974; 141:503-519.
9. Sun G, Shi YB Thyroid hormone regulation of adult intestinal stem cell development: mechanisms and evolutionary conservations. Int J Biol Sci. 2012; 8:1217-1224.
10. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell. 2013; 154:274-284.
11. Tata JR. Gene expression during metamorphosis: an ideal model for post-embryonic development. Bioessays. 1993; 15:239-248.
12. Shi Y-B. Amphibian Metamorphosis: From Morphology to Molecular Biology. New York, NY: John Wiley, Sons, Inc; 1999.
13. Ishizuya-Oka A., Shi YB Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis. Dev Dyn. 2007; 236:3358-3368.
14. Muncan V, Heijmans J, Krasinski S.D., et al. Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat Commun. 2011; 2:452.
15. Harper J, Mould A, Andrews R.M., Bikoff EK, Robertson EJ. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc Natl Acad Sci USA. 2011; 108:10585-10590.
16. Ishizuya-Oka A., Shimozawa A. Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis invitro. Roux's Arch Dev Biol. 1992; 201:322-329.
17. Ishizuya-Oka A., Shimozawa A. Inductive action of epithelium on differentiation of intestinal connective tissue of Xenopus laevis tadpoles during metamorphosis in vitro. Cell Tissue Res. 1994; 277: 427-436.
18. Hasebe T, Fu L, Miller T.C., Zhang Y., Shi YB, Ishizuya-Oka A. Thyroid hormone-induced cell-cell interactions are required for the development of adult intestinal stem cells. Cell Biosci. 2013; 3:18.
19. Schreiber AM, Mukhi S, Brown DD Cell-cell interactions during remodeling of the intestineatmetamorphosis in Xenopus laevis. Dev Biol. 2009; 331:89-98.
20. Schreiber AM, Cai L, Brown DD. Remodeling of the in testine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci USA. 2005; 102:3720-3725.
21. Ishizuya-Oka A., Hasebe T, Buchholz D.R., Kajita M., Fu L, Shi YB. Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis. FASEB J. 2009; 23:2568-2575.
22. Hasebe T, Buchholz DR, Shi Y.B., Ishizuya-Oka A. Epithelial-connective tissue interactions induced by thyroid hormone receptor are essential for adult stem cell development in the Xenopus laevis intestine. Stem Cells. 2011; 29:154-161.
23. Lazar MA. Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev. 1993; 14:184-193.
24. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001; 81:1097-1142.
25. Tsai MJ, O'Malley BW. Molecular mechanisms of action of steroid/ thyroid receptor superfamily members. Ann Rev Biochem. 1994; 63:451-486.
26. 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.
27. Shi YB, Matsuura K, Fujimoto K., Wen L, Fu L. Thyroid hormone receptor actions on transcription in amphibia: the roles of histone modification and chromatin disruption. Cell Biosci. 2012; 2:42.
28. Sun G, Fu L, Shi Y-B. Epigenetic regulation of thyroid hormoneinduced adult intestinal stem cell development during anuran metamorphosis. Cell Biosci. 2014; 4:73.
29. Wong J, Shi YB Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J Biol Chem. 1995; 270:18479-18483.
30. Wong J, Shi YB, Wolffe AP A role for nucleosome assembly in both silencing and activation of the Xenopus TR β A gene by the thyroid hormone receptor. Genes Dev. 1995; 9:2696-2711.
31. Burke LJ, Baniahmad A. Co-repressors 2000. FASEB J. 2000; 14: 1876-1888.
32. Jones PL, Shi YB N-CoR-HDAC corepressor complexes: roles in transcriptional regulation by nuclear hormone receptors. Curr Top Microbiol Immunol. 2003; 274:237-268.
33. Glass CK, Rosenfeld MG The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 2000; 14:121-141.
34. Zhang J, Lazar MA The mechanism of action of thyroid hormones. Annu Rev Physiol. 2000; 62:439-466.
35. Jones PL, Sachs LM, Rouse N, Wade P.A., Shi YB. Multiple N-CoR complexes contain distinct histone deacetylases. J Biol Chem. 2001; 276:8807-8811.
36. McKenna NJ, O'Malley BW. Nuclear receptors, coregulators, ligands, and selective receptor modulators: making sense of the patchwork quilt. Ann NY Acad Sci. 2001; 949:3-5.
37. Rachez C, Freedman LP Mediator complexes and transcription. Curr Opin Cell Biol. 2001; 13:274-280.
38. Puzianowska-Kuznicka M., Damjanovski S, Shi Y-B. Both thyroid hormone and 9-cis retinoic acid receptors are required to efficiently mediate the effects of thyroid hormone on embryonic development and specific gene regulation in Xenopus laevis. Mol And Cell Biol. 1997; 17:4738-4749.
39. Sachs LM, Shi YB Targeted chromatin binding and histone acetylation in vivo by thyroid hormone receptor during amphibian development. Proc Natl Acad Sci USA. 2000; 97:13138-13143.
40. Buchholz DR, Paul BD, Shi YB Gene-specific changes in promoter occupancy by thyroid hormone receptor during frog metamorphosis. Implications for developmental gene regulation. J Biol Chem. 2005; 280:41222-41228.
41. Nakajima K, Yaoita Y. Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn. 2003; 227:246-255.
42. Schreiber AM, Brown DD Tadpole skin dies autonomously in response to thyroid hormone at metamorphosis. Proc Natl Acad Sci USA. 2003; 100:1769-1774.
43. Das B, Schreiber AM, Huang H, Brown DD Multiple thyroid hormone-induced muscle growth and death programs during metamorphosis in Xenopus laevis. Proc NatlAcad Sci USA. 2002; 99:12230-12235.
44. 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. Proc Natl Acad Sci USA. 2001; 98:10739-10744.
45. Buchholz DR, Hsia SC, Fu L, Shi YB A dominant-negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Mol Cell Biol. 2003; 23:6750-6758.
46. Buchholz DR, Tomita A, Fu L., Paul BD, Shi YB. 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.
47. Grimaldi AG, Buisine N, Bilesimo P., Sachs LM. High-throughput sequencing will metamorphose the analysis of thyroid hormone receptor function during amphibian development. Curr Top Dev Biol. 2013; 103:277-303.
48. Denver RJ, Hu F, Scanlan T.S., Furlow JD. Thyroid hormone receptor subtype specificity for hormone-dependent neurogenesis in Xenopus laevis. Dev Biol. 2009; 326:155-168.
49. Sun G, Heimeier RA, Fu L, et al Expression profiling of intestinal tissues implicates tissue-specific genes and pathways essential for thyroid hormone-induced adult stem cell development. Endocrinology. 2013; 154:4396-4407.
50. Brown DD, Kies MW The mammalian metabolism of L-histidine. II. The enzymatic formation, stabilization, purification, and properties of 4(5)-imidazolone-5(4)-propionic acid, the product of urocanase activity. J Biol Chem. 1959; 234:3188-3191.
51. Snyder SH, Silva OL, Kies MW The mammalian metabolism of L-histidine. IV. Purification and properties of imidazolone propionic acid hydrolase. J Biol Chem. 1961; 236:2996-2998.
52. Tabor H, Silverman M, Mehler A.H., Daft FS, Bauer H. L-histidine conversion to a urinary glutamic acid derivative in folic-acid-deficient rats. J Amer Chem Soc. 1953; 75:756-757.
53. Luhby AL. Observations on the excretion of formiminoglutamic acid in folic acid deficiency in man. Clin Res Proc. 1957; 5:8-9.
54. Wang X, Matsuda H, Shi YB Developmental regulation and function of thyroid hormone receptors and 9-cis retinoic acid receptors during Xenopus tropicalis metamorphosis. Endocrinology. 2008; 149:5610-5618.
55. Fujimoto K, Matsuura K, Das B., Fu L, Shi YB. Direct activation of Xenopus iodotyrosine deiodinase by thyroid hormone receptor in the remodeling intestine during amphibian metamorphosis. Endocrinology. 2012; 153:5082-5089.
56. Matsuura K, Fujimoto K, Fu L., Shi YB. 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.
57. 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.
58. 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.
59. Sterling J, Fu L, Matsuura K., Shi Y-B. Cytological and morphological analyses reveal distinct features of intestinal development during Xenopus tropicalis metamorphosis. PLoS One. 2012; 7:e47407, 47401-47410.
60. Bilesimo P, Jolivet P, Alfama G., et al. Specific histone lysine 4 methylation patterns define TR-binding capacity and differentiate direct T3 responses. Mol Endocrinol. 2011; 25:225-237.
61. Nieuwkoop PD, Faber J. Normal table of Xenopus laevis. 1st ed. Amsterdam, The Netherlands: North Holland Publishing; 1956.
62. Wang Z, Brown DD Thyroid hormone-induced gene expression program for amphibian tail resorption. J Biol Chem. 1993; 268: 16270-16278.
63. Kanamori A, Brown DD The regulation of thyroid hormone receptor β genes by thyroid hormone in Xenopus laevis. J Biol Chem. 1992; 267:739-745.
64. Shi YB, Brown DD The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J Biol Chem. 1993; 268: 20312-20317.
65. Das B, Heimeier RA, Buchholz D.R., 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.
66. Okada M, Tazawa I, Nakajima K., Yaoita Y. Expression of the amelogenin gene in the skin of Xenopus tropicalis. Zoolog Sci. 2013; 30.
67. Hasebe T, Hartman R, Matsuda H., Shi YB. Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell Tissue Res. 2006; 324:105-116.
68. Hu W, Haamedi N, Lee M., Kinoshita T, Ohnuma S. The structure and development of Xenopus laevis cornea. Exp Eye Res. 2013; 116:109-128.
69. Sandelin A, Wasserman WW Prediction of nuclear hormone receptor response elements. Mol Endocrinol. 2005; 19:595-606.
70. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000; 16:276-277.
71. 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.
72. Ranjan M, Wong J, Shi YB Transcriptional repression of Xenopus TR β gene is mediated by a thyroid hormone response element located near the start site. J Biol Chem. 1994; 269:24699-24705.
73. Ishizuya-Oka A., Ueda S. Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res. 1996; 286:467-476.
74. Ishizuya-Oka A., Ueda S, Damjanovski S., Li Q, Liang VC, Shi YB Anteroposterior gradient of epithelial transformation during amphibian intestinal remodeling: immunohistochemical detection of intestinal fatty acid-binding protein. Dev Biol. 1997; 192:149-161.
75. Ishizuya-Oka A., Shimizu K, Sakakibara S., Okano H, Ueda S. Thyroid hormone-upregulated expression of Musashi-1 is specific for progenitor cells of the adult epithelium during amphibian gastrointestinal remodeling. J Cell Sci. 2003; 116:3157-3164.
76. Sun G, Hasebe T, Fujimoto K., et al. Spatio-temporal expression profile of stem cell-associated gene LGR5 in the intestine during thyroid hormone-dependent metamorphosis in Xenopus laevis. PLoS One. 2010; 5:e13605.
77. Choi J, Suzuki KT, Sakuma T, Shewade L., Yamamoto T, Buchholz DR. Unliganded thyroid hormone receptor α regulates developmental timing via gene repression as revealed by gene disruption in Xenopus tropicalis. Endocrinology. 2015; 156:735-744.
78. Wen L, Shi YB Unliganded thyroid hormone receptor α controls developmental timing in Xenopus tropicalis. Endocrinology. 2015; 156:721-734.
79. Wong J, Shi YB, 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.
80. Plateroti M, Gauthier K, Domon-Dell C, Freund J.N., Samarut J., Chassande O. Functional interference between thyroid hormone receptor α (TRα) and natural truncated TRΔα isoforms in the control of intestine development. Mol Cell Biol. 2001; 21:4761-4772.
81. Flamant F, Poguet AL, Plateroti M, et al Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TRa gene. Mol Endocrinol. 2002; 16:24-32.
82. Kress E, Rezza A, Nadjar J., Samarut J, Plateroti M. The frizzledrelated sFRP2 gene is a target of thyroid hormone receptor α1 and activates β-catenin signaling in mouse intestine. J Biol Chem. 2009; 284:1234-1241.
83. Plateroti M, Chassande O, Fraichard A., et al. Involvement of T3Rα-and β-receptor subtypes in mediation of T3 functions during postnatal murine intestinal development. Gastroenterology. 1999; 116: 1367-1378.
84. Heimeier RA, Das B, Buchholz D.R., Fiorentino M., Shi YB. Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome Biol. 2010; 11:R55.
85. Dodd MHI, Dodd JM The biology of metamorphosis. In: Lofts B, ed. Physiology of the Amphibia. New York, NY: Academic Press; 1976:467-599.
86. Luu N, Wen L, Fu L., Fujimoto K, Shi YB, Sun G. Differential regulation of two histidine ammonia-lyase genes during Xenopus development implicates distinct functions during thyroid hormoneinduced formation of adult stem cells. Cell Biosci. 2013; 3:43.
87. Kawai Y, Moriyama A, Asai K., et al. Molecular characterization of histidinemia: identification of four missense mutations in the histidase gene. Hum Genet. 2005; 116:340-346.
88. Suchi M, Harada N, Wada Y., Takagi Y. Molecular cloning of a cDNA encoding human histidase. Biochim Biophys Acta. 1993; 1216:293-295.
89. Suchi M, Sano H, Mizuno H, Wada Y. Molecular cloning and structural characterization of the human histidase gene (HAL). Genomics. 1995; 29:98-104.
90. Taylor RG, Levy HL, McInnes RR Histidase and histidinemia. Clinical and molecular considerations. Mol Biol Med. 1991; 8:101-116.
91. Wang J, Alexander P, Wu L., Hammer R, Cleaver O, McKnight SL Dependence of mouse embryonic stem cells on threonine catabolism. Science. 2009; 325:435-439.