Abstract
Thyroid hormone is known to participate in the control of intestine maturation at weaning. Its action is mediated by the thyroid hormone nuclear receptors, encoded by the TRalpha and TRbeta genes. Since previous studies have shown that TRbeta plays a minor role in the gut, we focused here our analysis on the TRalpha gene. The TRalpha locus generates the TRalpha1 receptor together with the splicing variant TRalpha2 and the truncated products TRDeltaalpha1 and TRDeltaalpha2, which all lack an intact ligand binding domain. The TRDeltaalpha isoforms are transcribed from an internal promoter located in intron 7, and their distribution is restricted to a few tissues including those of the intestine. In order to define the functions of the different isoforms encoded by the TRalpha locus in the intestinal mucosa, we produced mice either lacking all known TRalpha products or harboring a mutation which inactivates the intronic promoter. We performed a detailed analysis of the intestinal phenotypes in these mice and compared it to that of the previously described TRalpha(-/-) mice, in which TRalpha isoforms are abolished but the TRDeltaalpha isoforms remain. This comparative analysis leads us to the following conclusions: (i) the TRalpha1 receptor mediates the T3-dependent functions in the intestine at weaning time and (ii) the TRDeltaalpha products negatively control the responsiveness of the epithelial cells to T3. Moreover, we show that TRDeltaalpha proteins can interfere with the transcription of the intestine-specific homeobox genes cdx1 and cdx2 and that their activity is regulated by TRalpha1. Altogether these data demonstrate that cooperation of TRalpha and TRDeltaalpha products is essential to ensure the normal postnatal development of the intestine and that mutations in the TRalpha locus can generate different phenotypes caused by the disruption of the equilibrium between these products.
MeSH Terms
Animals
Avian Proteins
CDX2 Transcription Factor
Cell Differentiation
Cell Division
Gene Expression Profiling
Gene Expression Regulation
Gene Targeting
Homeodomain Proteins/genetics
Humans
Intestinal Mucosa/metabolism,pathology
Intestine, Small/growth & development,pathology,physiology
Mice
Mice, Knockout
Protein Isoforms/biosynthesis,genetics,metabolism,physiology
RNA, Messenger
Receptors, Thyroid Hormone/biosynthesis,genetics,metabolism,physiology
Trans-Activators
Triiodothyronine/metabolism
Chemicals
Avian Proteins
CDX1 protein, human
CDX2 Transcription Factor
CDX2 protein, human
Cdx1 protein, mouse
Homeodomain Proteins
Protein Isoforms
RNA, Messenger
Receptors, Thyroid Hormone
Trans-Activators
Triiodothyronine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Plateroti M
Laboratoire de Biologie Moléculaire et Cellulaire de l'ENS de Lyon, UMR 5665 CNRS, LA 913 INRA, 69364 Lyon Cedex 07, France.
Gauthier K
Domon-Dell C
Freund J N
Samarut J
Chassande O
References (29)
29 references, click to expand
-
Functions of thyroid hormone receptors in mice.
Thyroid. 2000 Jan;10(1):41-52
PMID: 10691312
-
Intestinal mucosal hyperplasia following induced hyperthyroidism in the rat.
Virchows Arch B Cell Pathol. 1970;6(2):79-87
PMID: 4319200
-
Cloning and characterization of two novel thyroid hormone receptor beta isoforms.
Mol Cell Biol. 2000 Nov;20(22):8329-42
PMID: 11046130
-
Increased sensitivity to thyroid hormone in mice with complete deficiency of thyroid hormone receptor alpha.
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):349-54
PMID: 11120878
-
Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus.
Mol Cell Biol. 2001 Jul;21(14):4748-60
PMID: 11416150
-
Development of the small intestine in the hypophysectomized rat. II. Influence of cortisone, thyroxine, growth hormone, and prolactin.
Dev Biol. 1975 Nov;47(1):173-84
PMID: 173593
-
Goblet cells in embryonic intestine: accelerated differentiation in culture.
Science. 1977 Jul 22;197(4301):368-70
PMID: 560059
-
Control of brush border enzymes by dexamethasone in the fetal rat intestine cultured in vitro.
J Pediatr Gastroenterol Nutr. 1982;1(2):257-65
PMID: 6821111
-
Epithelial properties of human colonic carcinoma cell line Caco-2: electrical parameters.
Am J Physiol. 1984 Sep;247(3 Pt 1):C260-7
PMID: 6476109
-
The c-erb-A protein is a high-affinity receptor for thyroid hormone.
Nature. 1986 Dec 18-31;324(6098):635-40
PMID: 2879242
-
The c-erb-A gene encodes a thyroid hormone receptor.
Nature. 1986 Dec 18-31;324(6098):641-6
PMID: 2879243
-
Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing.
Nature. 1989 Feb 16;337(6208):659-61
PMID: 2537467
-
Intestinal epithelial differentiation: new insights from chimeric and transgenic mice.
J Cell Biol. 1989 Apr;108(4):1187-94
PMID: 2647764
-
Human carboxyl-terminal variant of alpha-type c-erbA inhibits trans-activation by thyroid hormone receptors without binding thyroid hormone.
Proc Natl Acad Sci U S A. 1989 Oct;86(20):7771-4
PMID: 2554288
-
Pituitary regulation of postnatal small intestinal ontogeny in the rat: differential regulation of digestive hydrolase maturation by thyroxine and growth hormone.
Endocrinology. 1991 Sep;129(3):1417-23
PMID: 1874180
-
Gene expression during metamorphosis: an ideal model for post-embryonic development.
Bioessays. 1993 Apr;15(4):239-48
PMID: 8517853
-
Thyroid hormone receptors: multiple forms, multiple possibilities.
Endocr Rev. 1993 Apr;14(2):184-93
PMID: 8325251
-
The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins.
J Cell Biol. 1993 Nov;123(3):513-22
PMID: 8227122
-
Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation.
J Cell Sci. 1994 Jan;107 ( Pt 1):213-25
PMID: 8175910
-
Expression of thyroid hormone receptor isoforms in rat oligodendrocyte cultures. Effect of 3,5,3'-triiodo-L-thyronine.
Neurosci Lett. 1994 Jul 18;176(1):47-51
PMID: 7970235
-
Pattern of rat intestinal brush-border enzyme gene expression changes with epithelial growth state.
Am J Physiol. 1995 Aug;269(2 Pt 1):C385-91
PMID: 7653520
-
Thyroid hormone and the gut: selective transcriptional activation of a villus-enterocyte marker.
Surgery. 1996 Aug;120(2):138-43
PMID: 8751575
-
The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production.
EMBO J. 1997 Jul 16;16(14):4412-20
PMID: 9250685
-
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. 1997 Aug;11(9):1278-90
PMID: 9259319
-
Downregulation of the colon tumour-suppressor homeobox gene Cdx-2 by oncogenic ras.
Oncogene. 1999 Jan 7;18(1):87-92
PMID: 9926923
-
Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development.
EMBO J. 1999 Feb 1;18(3):623-31
PMID: 9927422
-
Involvement of T3Ralpha- and beta-receptor subtypes in mediation of T3 functions during postnatal murine intestinal development.
Gastroenterology. 1999 Jun;116(6):1367-78
PMID: 10348820
-
The Cdx-1 and Cdx-2 homeobox genes in the intestine.
Biochem Cell Biol. 1998;76(6):957-69
PMID: 10392709
-
Retinoic acid regulation of Cdx1: an indirect mechanism for retinoids and vertebral specification.
Mol Cell Biol. 2000 Sep;20(17):6579-86
PMID: 10938132