Thyroid hormones and their nuclear receptors: New players in intestinal epithelium stem cell biology?

Cellular and Molecular Life Sciences

Volumn 71, Issue 15, 2014, Pages 2897-2907

  Sirakov, Maria ^b   Kress, Elsa ^a   Nadjar, Julien ^a   Plateroti, Michelina ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Intestinal epithelium; Intestine; Stem cells; Thyroid hormone; Thyroid hormone receptor TR

Indexed keywords

LIOTHYRONINE; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; THYROXINE 5 DEIODINASE;

CANCER THERAPY; CARCINOGENESIS; CELL FUNCTION; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; CONSTIPATION; DISEASE ASSOCIATION; GASTROINTESTINAL MUCOSA; GENE MUTATION; HOMEOSTASIS; HUMAN; HYPOTHYROIDISM; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; LIOTHYRONINE BLOOD LEVEL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TISSUE ENGINEERING; WNT SIGNALING PATHWAY;

AMPHIBIA; MAMMALIA;

ANIMALS; HOMEOSTASIS; HUMANS; INTESTINAL MUCOSA; NEOPLASMS; RECEPTORS, THYROID HORMONE; STEM CELLS; THYROID HORMONES; WNT SIGNALING PATHWAY;

EID: 84904384467     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1586-3     Document Type: Review

References (111)

1. Yen PM, Ando S, Feng X, Liu Y, Maruvada P, Xia X (2006) Thyroid hormone action at the cellular, genomic and target gene levels. Mol Cell Endocrinol 246(1-2):121-127 (Pubitemid 43238405)
2. Tata JR (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol Cell Endocrinol 246(1-2):10-20
3. Fredric E, Wondisford M (2004) Lessons learned from TR-beta mutant mice. In: Beck-Peccoz P (ed) Syndromes of hormone resistance on the hypothalamic-pituitary-thyroid axis, Kluwer Academic Publishers,Uttar Pradesh, India, pp 109-118
4. Dumitrescu AM, Liao XH, Weiss RE, Millen K, Refetoff S (2006) Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology 147(9):4036-4043 (Pubitemid 44268357)
5. Refetoff S, Dumitrescu AM (2007) Syndromes of reduced sensitivity to thyroid hormone: genetic defects in hormone receptors, cell transporters and deiodination. Best Pract Res Clin Endocrinol Metab 21(2):277-305 (Pubitemid 46888195)
6. Friesema EC, Grueters A, Biebermann H, Krude H, von Moers A, Reeser M, Barrett TG, Mancilla E, Svensson J, Kester MH, Kuiper GG, Balkassmi S, Uitterlinden AG, Koehrle J, Rodien P, Halestrap AP, Visser TJ (2004) Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet 364(9443):1435-1437 (Pubitemid 39370719)
7. Visser TJ (2007) Thyroid hormone transporters. Horm Res 68(Suppl 5):28-30
8. Bianco AC, Kim BW (2006) Deiodinases: implications of the local control of thyroid hormone action. J Clin Invest 116(10):2571-2579 (Pubitemid 44511617)
9. Laudet V (1997) Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J Mol Endocrinol 19(3):207-226
10. Koenig RJ, Lazar MA, Hodin RA, Brent GA, Larsen PR, Chin W, Moore DD (1989) Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing. Nature 337(6208):659-661 (Pubitemid 19054295)
11. Hartong R, Wang N, Kurokawa R, Lazar MA, Glass CK, Apriletti JW, Dillmann WH (1994) Delineation of three different thyroid hormone-response elements in promoter of rat sarcoplasmic reticulum Ca2 + ATPase gene. Demonstration that retinoid X receptor binds 5′ to thyroid hormone receptor in response element 1. J Biol Chem 269(17):13021-13029 (Pubitemid 24202107)
12. Sirakov M, Plateroti M (2011) The thyroid hormones and their nuclear receptors in the gut: from developmental biology to cancer. Biochim Biophys Acta 1812(8):938-946
13. Sirakov M, Skah S, Nadjar J, Plateroti M (2013) Thyroid hormone's action on progenitor/stem cell biology: new challenge for a classic hormone? Biochim Biophys Acta 1830(7):3917-3927
14. Davis PJ, Leonard JL, Davis FB (2008) Mechanisms of non-genomic actions of thyroid hormone. Front Neuroendocrinol 29(2):211-218 (Pubitemid 351467119)
15. Davis PJ, Davis FB, Mousa SA, Luidens MK, Lin HY (2011) Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu Rev Pharmacol Toxicol 51:99-115
16. Lazar MA (2003) Thyroid hormone action: a binding contract. J Clin Invest 112(4):497-499 (Pubitemid 38056333)
17. Tata JR (2011) Looking for the mechanism of action of thyroid hormone. J Thyroid Res 2011:730630
18. Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31(2):139-170
19. Brent GA (2012) Mechanisms of thyroid hormone action. J Clin Invest 122(9):3035-3043
20. Pascual A, Aranda A (2013) Thyroid hormone receptors, cell growth and differentiation. Biochim Biophys Acta 1830(7):3908-3916
21. van der Flier LG, Clevers H (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71:241-260
22. 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(7229):608-611
23. Puzianowska-Kuznicka M, Pietrzak M, Turowska O, Nauman A (2006) Thyroid hormones and their receptors in the regulation of cell proliferation. Acta Biochim Pol 53(4):641-650 (Pubitemid 46090114)
24. Su Y, Damjanovski S, Shi Y, Shi YB (1999) Molecular and cellular basis of tissue remodeling during amphibian metamorphosis. Histol Histopathol 14(1):175-183 (Pubitemid 29049366)
25. Santisteban P, Bernal J (2005) Thyroid development and effect on the nervous system. Rev Endocr Metab Disord 6(3):217-228 (Pubitemid 41285599)
26. Patel J, Landers K, Li H, Mortimer RH, Richard K (2011) Thyroid hormones and fetal neurological development. J Endocrinol 209(1):1-8
27. Mohan V, Sinha RA, Pathak A, Rastogi L, Kumar P, Pal A, Godbole MM (2012) Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Exp Neurol 237(2):477-488
28. Chen C, Zhou Z, Zhong M, Zhang Y, Li M, Zhang L, Qu M, Yang J, Wang Y, Yu Z (2012) Thyroid hormone promotes neuronal differentiation of embryonic neural stem cells by inhibiting STAT3 signaling through TRalpha1. Stem Cells Dev 21(14):2667-2681
29. Lemkine GF, Raj A, Alfama G, Turque N, Hassani Z, Alegria-Prevot O, Samarut J, Levi G, Demeneix BA (2005) Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. Faseb J 19(7):863-865 (Pubitemid 40617410)
30. Lopez-Juarez A, Remaud S, Hassani Z, Jolivet P, Pierre SJ, Sontag T, Yoshikawa K, Price J, Morvan-Dubois G, Demeneix BA (2012) Thyroid hormone signaling acts as a neurogenic switch by repressing Sox2 in the adult neural stem cell niche. Cell Stem Cell 10(5):531-543
31. Kapoor R, Ghosh H, Nordstrom K, Vennstrom B, Vaidya VA (2011) Loss of thyroid hormone receptor beta is associated ith increased progenitor proliferation and NeuroD-positive cell number in the adult hippocampus. Neurosci Lett 487(2):199-203
32. Kapoor R, Desouza LA, Nanavaty IN, Kernie SG, Vaidya VA (2012) Thyroid hormone accelerates the differentiation of adult hippocampal progenitors. J Neuroendocrinol 24(9):1259-1271
33. Tiede S, Bohm K, Meier N, Funk W, Paus R (2010) Endocrine controls of primary adult human stem cell biology: thyroid hormones stimulate keratin 15 expression, apoptosis, and differentiation in human hair follicle epithelial stem cells in situ and in vitro. Eur J Cell Biol 89(10):769-777
34. Lee YK, Ng KM, Chan YC, Lai WH, Au KW, Ho CY, Wong LY, Lau CP, Tse HF, Siu CW (2010) Triiodothyronine promotes cardiac differentiation and maturation of embryonic stem cells via the classical genomic pathway. Mol Endocrinol 24(9):1728-1736
35. Henning SJ, Rudbin DC, Shulman J (1994) Ontogeny of the intestinal mucosa. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 3rd edn. Raven Press, New York, pp 571-601
36. Heimeier RA, Das B, Buchholz DR, Fiorentino M, Shi YB (2010) Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome Biol 11(5):R55
37. Kress E, Rezza A, Nadjar J, Samarut J, Plateroti M (2009) The frizzled-related sFRP2 gene is a target of thyroid hormone receptor alpha1 and activates beta-catenin signaling in mouse intestine. J Biol Chem 284(2):1234-1241
38. Kress E, Skah S, Sirakov M, Nadjar J, Gadot N, Scoazec JY, Samarut J, Plateroti M (2010) Cooperation between the thyroid hormone receptor TRalpha1 and the WNT pathway in the induction of intestinal tumorigenesis. Gastroenterology 138(5):1863-1874
39. Randall D, Burggren W, French K (2002) Eckert Animal Physiology mechanisms and adaptation. Freeman and Company, New York
40. Gerbe F, Legraverend C, Jay P (2012) The intestinal epithelium tuft cells: specification and function. Cell Mol Life Sci 69(17):2907-2917
41. Stappenbeck TS, Wong MH, Saam JR, Mysorekar IU, Gordon JI (1998) Notes from some crypt watchers: regulation of renewal in the mouse intestinal epithelium. Curr Opin Cell Biol 10(6):702-709 (Pubitemid 28561013)
42. Ishizuya-Oka A, Shi YB (2008) Thyroid hormone regulation of stem cell development during intestinal remodeling. Mol Cell Endocrinol 288(1-2):71-78
43. Sancho E, Batlle E, Clevers H (2004) Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol 20:695-723 (Pubitemid 39488655)
44. Kress E, Samarut J, Plateroti M (2009) Thyroid hormones and the control of cell proliferation or cell differentiation: paradox or duality? Mol Cell Endocrinol 313(1-2):36-49
45. Buchholz DR, Heimeier RA, Das B, Washington T, Shi YB (2007) Pairing morphology with gene expression in thyroid hormone-induced intestinal remodeling and identification of a core set of TH-induced genes across tadpole tissues. Dev Biol 303(2):576-590 (Pubitemid 46350760)
46. Barker N, Clevers H (2010) Lineage tracing in the intestinal epithelium. Curr Protoc Stem Cell Biol, Chp. 5:Unit5A 4
47. Cheng H, Leblond CP (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat 141(4):461-479
48. Chwalinski S, Potten CS, Evans G (1988) Double labelling with bromodeoxyuridine and [3H]-thymidine of proliferative cells in small intestinal epithelium in steady state and after irradiation. Cell Tissue Kinet 21(5):317-329 (Pubitemid 19122829)
49. Potten CS (1977) Extreme sensitivity of some intestinal crypt cells to X and gamma irradiation. Nature 269(5628):518-521
50. Bjerknes M, Cheng H (1999) Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116(1):7-14 (Pubitemid 29013487)
51. 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(7165):1003-1007 (Pubitemid 350014593)
52. Schepers AG, Vries R, van den Born M, van de Wetering M, Clevers H (2011) Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J 30(6):1104-1109
53. Montgomery RK, Carlone DL, Richmond CA, Farilla L, Kranendonk ME, Henderson DE, Baffour-Awuah NY, Ambruzs DM, Fogli LK, Algra S, Breault DT (2011) Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc Natl Acad Sci USA 108(1):179-184
54. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40(7):915-920 (Pubitemid 351913652)
55. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423(6937):255-260 (Pubitemid 40852690)
56. Takeda N, Jain R, LeBoeuf MR, Wang Q, Lu MM, Epstein JA (2011) Interconversion between intestinal stem cell populations in distinct niches. Science 334(6061):1420-1424
57. Cambuli FM, Rezza A, Nadjar J, Plateroti M (2013) Musashi1-Egfp Mice, a new tool for differential isolation of the intestinal stem cell populations. Stem Cells 31(10):5
58. Carlone DL, Breault DT (2012) Tales from the crypt: the expanding role of slow cycling intestinal stem cells. Cell Stem Cell 10(1):2-4
59. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143(1):134-144
60. Ishizuya-Oka A, Shi YB (2005) Molecular mechanisms for thyroid hormone-induced remodeling in the amphibian digestive tract: a model for studying organ regeneration. Dev Growth Differ 47(9):601-607 (Pubitemid 43151676)
61. Hadj-Sahraoui N, Seugnet I, Ghorbel MT, Demeneix B (2000) Hypothyroidism prolongs mitotic activity in the post-natal mouse brain. Neurosci Lett 280(2):79-82 (Pubitemid 30109137)
62. Cai L, Brown DD (2004) Expression of type II iodothyronine deiodinase marks the time that a tissue responds to thyroid hormone-induced metamorphosis in Xenopus laevis. Dev Biol 266(1):87-95 (Pubitemid 38083197)
63. Bates JM, Germain DL, Galton VA (1999) Expression profiles of the three iodothyronine deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 140(2):844-851 (Pubitemid 29058221)
64. Sirakov M, Skah S, Lone IN, Nadjar J, Angelov D, Plateroti M (2012) Multi-level interactions between the nuclear receptor TRalpha1 and the WNT effectors beta-catenin/Tcf4 in the intestinal epithelium. PLoS One 7(4):e34162
65. Das B, Matsuda H, Fujimoto K, Sun G, Matsuura K, Shi YB (2010) Molecular and genetic studies suggest that thyroid hormone receptor is both necessary and sufficient to mediate the developmental effects of thyroid hormone. Gen Comp Endocrinol 168(2):174-180
66. Plateroti M, Chassande O, Fraichard A, Gauthier K, Freund JN, Samarut J, Kedinger M (1999) Involvement of T3Ralpha- and beta-receptor subtypes in mediation of T3 functions during postnatal murine intestinal development. Gastroenterology 116(6):1367-1378 (Pubitemid 29258885)
67. Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, Rousset B, Weiss R, Trouillas J, Samarut J (1999) Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J 18(3):623-631 (Pubitemid 29057247)
68. Hodin RA, Meng S, Chamberlain SM (1994) Thyroid hormone responsiveness is developmentally regulated in the rat small intestine: a possible role for the alpha-2 receptor variant. Endocrinology 135(2):564-568 (Pubitemid 24241234)
69. Plateroti M, Kress E, Mori JI, Samarut J (2006) Thyroid hormone receptor alpha1 directly controls transcription of the beta-catenin gene in intestinal epithelial cells. Mol Cell Biol 26(8):3204-3214
70. Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, Willott JF, Sundin V, Roux JP, Malaval L, Hara M, Samarut J, Chassande O (2001) Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol 21(14):4748-4760 (Pubitemid 32588255)
71. Jumarie C, Malo C (1994) Alkaline phosphatase and peptidase activities in Caco-2 cells: differential response to triiodothyronine. Vitro Cell Dev Biol Anim 30A(11):753-760 (Pubitemid 24376739)
72. Matosin-Matekalo M, Mesonero JE, Laroche TJ, Lacasa M, Brot-Laroche E (1999) Glucose and thyroid hormone co-regulate the expression of the intestinal fructose transporter GLUT5. Biochem J 339(Pt 2):233-239 (Pubitemid 29209952)
73. Bochukova E, Schoenmakers N, Agostini M, Schoenmakers E, Rajanayagam O, Keogh JM, Henning E, Reinemund J, Gevers E, Sarri M, Downes K, Offiah A, Albanese A, Halsall D, Schwabe JW, Bain M, Lindley K, Muntoni F, Khadem FV, Dattani M, Farooqi IS, Gurnell M, Chatterjee K (2012) A mutation in the thyroid hormone receptor alpha gene. N Engl J Med 366(3):243-249
74. van Mullem A, van Heerebeek R, Chrysis D, Visser E, Medici M, Andrikoula M, Tsatsoulis A, Peeters R, Visser TJ (2012) Clinical phenotype and mutant TRalpha1. N Engl J Med 366(15):1451-1453
75. Furness JB (2012) The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9(5):286-294
76. Fraichard A, Chassande O, Plateroti M, Roux JP, Trouillas J, Dehay C, Legrand C, Gauthier K, Kedinger M, Malaval L, Rousset B, Samarut J (1997) The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J 16(14):4412-4420 (Pubitemid 27298194)
77. Plateroti M, Gauthier K, Domon-Dell C, Freund JN, Samarut J, Chassande O (2001) Functional interference between thyroid hormone receptor alpha (TRalpha) and natural truncated TRDeltaalpha isoforms in the control of intestine development. Mol Cell Biol 21(14):4761-4772 (Pubitemid 32588256)
78. Wikstrom L, Johansson C, Salto C, Barlow C, Campos BA, Baas F, Forrest D, Thoren P, Vennstrom B (1998) Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J 17(2):455-461 (Pubitemid 28045486)
79. Chassande O, Fraichard A, Gauthier K, Flamant F, Legrand C, Savatier P, Laudet V, Samarut J (1997) Identification of transcripts initiated from an internal promoter in the c-erbA alpha locus that encode inhibitors of retinoic acid receptor-alpha and triiodothyronine receptor activities. Mol Endocrinol 11(9):1278-1290 (Pubitemid 28041335)
80. Gonzalez-Sancho JM, Garcia V, Bonilla F, Munoz A (2003) Thyroid hormone receptors/THR genes in human cancer. Cancer Lett 192(2):121-132 (Pubitemid 36369266)
81. Horkko TT, Tuppurainen K, George SM, Jernvall P, Karttunen TJ, Makinen MJ (2006) Thyroid hormone receptor beta1 in normal colon and colorectal cancer-association with differentiation, polypoid growth type and K-ras mutations. Int J Cancer 118(7):1653-1659 (Pubitemid 43376428)
82. Cheng SY (2003) Thyroid hormone receptor mutations in cancer. Mol Cell Endocrinol 213(1):23-30
83. Rose DP, Davis TE (1981) Plasma thyronine levels in carcinoma of the breast and colon. Arch Intern Med 141(9):1161-1164 (Pubitemid 11017499)
84. Wang CS, Lin KH, Hsu YC (2002) Alterations of thyroid hormone receptor alpha gene: frequency and association with Nm23 protein expression and metastasis in gastric cancer. Cancer Lett 175(2):121-127
85. Iishi H, Tatsuta M, Baba M, Okuda S, Taniguchi H (1992) Enhancement by thyroxine of experimental carcinogenesis induced in rat colon by azoxymethane. Int J Cancer 50(6):974-976
86. Lin KH, Zhu XG, Hsu HC, Chen SL, Shieh HY, Chen ST, McPhie P, Cheng SY (1997) Dominant negative activity of mutant thyroid hormone alpha1 receptors from patients with hepatocellular carcinoma. Endocrinology 138(12):5308-5315 (Pubitemid 27509692)
87. Lin KH, Zhu XG, Shieh HY, Hsu HC, Chen ST, McPhie P, Cheng SY (1996) Identification of naturally occurring dominant negative mutants of thyroid hormone alpha 1 and beta 1 receptors in a human hepatocellular carcinoma cell line. Endocrinology 137(10):4073-4081 (Pubitemid 26321847)
88. Brown AR, Simmen RC, Simmen FA (2013) The role of thyroid hormone signaling in the prevention of digestive system cancers. Int J Mol Sci 14(8):16240-16257
89. Wu SM, Huang YH, Yeh CT, Tsai MM, Liao CH, Cheng WL, Chen WJ, Lin KH (2011) Cathepsin H regulated by the thyroid hormone receptors associate with tumor invasion in human hepatoma cells. Oncogene 30(17):2057-2069
90. Dentice M, Luongo C, Huang S, Ambrosio R, Elefante A, Mirebeau-Prunier D, Zavacki AM, Fenzi G, Grachtchouk M, Hutchin M, Dlugosz AA, Bianco AC, Missero C, Larsen PR, Salvatore D (2007) Sonic hedgehog-induced type 3 deiodinase blocks thyroid hormone action enhancing proliferation of normal and malignant keratinocytes. Proc Natl Acad Sci USA 104(36):14466-14471 (Pubitemid 350003284)
91. Dentice M, Luongo C, Ambrosio R, Sibilio A, Casillo A, Iaccarino A, Troncone G, Fenzi G, Larsen PR, Salvatore D (2010) beta-Catenin regulates deiodinase levels and thyroid hormone signaling in colon cancer cells. Gastroenterology 143(4):1037-1047
92. Modica S, Gofflot F, Murzilli S, D'Orazio A, Salvatore L, Pellegrini F, Nicolucci A, Tognoni G, Copetti M, Valanzano R, Veschi S, Mariani-Costantini R, Palasciano G, Schoonjans K, Auwerx J, Moschetta A (2009) The intestinal nuclear receptor signature with epithelial localization patterns and expression modulation in tumors. Gastroenterology 138(2):636-648
93. Markowitz S, Haut M, Stellato T, Gerbic C, Molkentin K (1989) Expression of the ErbA-beta class of thyroid hormone receptors is selectively lost in human colon carcinoma. J Clin Invest 84(5):1683-1687 (Pubitemid 19272261)
94. Thompson JS, Saxena SK, Sharp JG (2000) Regulation of intestinal regeneration: new insights. Microsc Res Tech 51(2):129-137
95. Koch S, Nusrat A (2012) The life and death of epithelia during inflammation: lessons learned from the gut. Annu Rev Pathol 7:35-60
96. Kress E, Rezza A, Nadjar J, Samarut J, Plateroti M (2008) The thyroid hormone receptor-alpha (TRalpha) gene encoding TRalpha1 controls deoxyribonucleic acid damage-induced tissue repair. Mol Endocrinol 22(1):47-55
97. Park HS, Goodlad RA, Wright NA (1995) Crypt fission in the small intestine and colon. A mechanism for the emergence of G6PD locus-mutated crypts after treatment with mutagens. Am J Pathol 147(5):1416-1427
98. Snippert HJ, Schepers AG, van Es JH, Simons BD, Clevers H (2014) Biased competition between Lgr5 intestinal stem cells driven by oncogenic mutation induces clonal expansion. EMBO Rep 15(1):62-69
99. Ishizuya-Oka A, Hasebe T, Buchholz DR, Kajita M, Fu L, Shi YB (2009) Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis. FASEB J 23(8):2568-2575
100. Shi YB, Hasebe T, Fu L, Fujimoto K, Ishizuya-Oka A (2011) The development of the adult intestinal stem cells: insights from studies on thyroid hormone-dependent amphibian metamorphosis. Cell Biosci 1(1):30
101. Rezza A, Skah S, Roche C, Nadjar J, Samarut J, Plateroti M (2010) The overexpression of the putative gut stem cell marker Musashi-1 induces tumorigenesis through Wnt and Notch activation. J Cell Sci 123(Pt 19):3256-3265
102. 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(2):241-250 (Pubitemid 35292444)
103. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127(3):469-480
104. MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17(1):9-26
105. Liu T, Lee YN, Malbon CC, Wang HY (2002) Activation of the beta-catenin/Lef-Tcf pathway is obligate for formation of primitive endoderm by mouse F9 totipotent teratocarcinoma cells in response to retinoic acid. J Biol Chem 277(34):30887-30891 (Pubitemid 34970789)
106. Fre S, Pallavi SK, Huyghe M, Lae M, Janssen KP, Robine S, Artavanis-Tsakonas S, Louvard D (2009) Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci USA 106(15):6309-6314
107. Kawano Y, Kypta R (2003) Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116(Pt 13):2627-2634 (Pubitemid 36857216)
108. Ord W (1878) On myxoedema, a term proposed to be applied to an essential condition in the "cretinoid" affection occasionally observed in middle-aged women. Med Chir Trans (Lond) 61:57
109. Horsley V (1885) The brown lectures on pathology. Br Med J 1:111-115
110. Pitt-Rivers R (1963) Biochemistry and physiology of thyroid hormones. NY State J Med 63:43-49
111. Ross DS (1994) Hyperthyroidism, thyroid hormone therapy, and bone. Thyroid 4(3):319-326