Development, Vol 112, Issue 4 933-943, Copyright © 1991 by Company of Biologists

JOURNAL ARTICLES

Developmental and regional expression of thyroid hormone receptor genes during Xenopus metamorphosis

A Kawahara, BS Baker and JR Tata
Laboratory of Developmental Biochemistry, National Institute for Medical Research, Mill Hill, London, UK.

A characteristic feature of the obligatory control of amphibian metamorphosis by thyroid hormones is the early acquisition of response of tadpole tissues to these hormones well before the latter are secreted, with 'exponentially' increasing hormonal sensitivity upon the onset of metamorphosis. We have therefore analyzed the expression of the two thyroid hormone receptor genes (TR alpha and beta) before, during and after metamorphosis in Xenopus tadpoles and froglets. Using non-cross-hybridizing cRNA probes for 5' and 3' sequences of Xenopus TR alpha and beta transcripts for RNAase protection assays, the two mRNAs can be detected in tadpoles as early as stage 39. Their concentration increases abruptly at stage 44 and continues to increase differentially at the onset of metamorphosis (stage 55) and through metamorphic climax at stages 58-62, after which they decline upon completion of metamorphosis at stage 66. Quantitative densitometric scanning of autoradiograms showed that, although the concentration of TR beta transcripts is about 1/30th of that of TR alpha mRNA at stages 44-48, depending on the region, it accumulates 3-10 times more rapidly than does the alpha isoform during further development. A substantial proportion of the increase in TR beta mRNA is localized to the head region of tadpoles. Using the hormone-binding domain (HBD) and 3' end of Xenopus TR alpha cRNA as probe for in situ hybridization, the highest concentration of TR transcripts in stage 44 tadpoles is seen in the brain and spinal cord. High concentrations of mRNA are also present in the intestinal epithelium and tail tip, tissues programmed for regression. At later stages (55 onwards), strong hybridization signals are also exhibited by hindlimb buds. This pattern persists through metamorphic climax, after which TR mRNAs decline in all tissues to low levels in froglets at stage 66. In developing froglets, TR transcripts were detected in large amounts in the cytoplasm of stage 1 and 2 oocytes but the rate of their accumulation did not increase with further oocyte growth. This observation raises the possibility that the response to thyroid hormones at early stages of tadpoles (42-44) may be due to TR synthesized on maternally derived mRNA. Exposure of tadpoles at premetamorphic stages (48-52) to exogenous thyroid hormone (T3) substantially enhanced the accumulation of TR mRNA, especially that of TR beta message, which could explain the accelerated increase in sensitivity of tadpoles to thyroid hormones at the onset of natural metamorphosis.(ABSTRACT TRUNCATED AT 400 WORDS)
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				X. Wang, H. Matsuda, and Y.-B. Shi Developmental Regulation and Function of Thyroid Hormone Receptors and 9-cis Retinoic Acid Receptors during Xenopus tropicalis Metamorphosis Endocrinology, November 1, 2008; 149(11): 5610 - 5618. [Abstract] [Full Text] [PDF]

				N. Saelim, L. M. John, J. Wu, J. S. Park, Y. Bai, P. Camacho, and J. D. Lechleiter Nontranscriptional modulation of intracellular Ca2+ signaling by ligand stimulated thyroid hormone receptor J. Cell Biol., December 6, 2004; 167(5): 915 - 924. [Abstract] [Full Text] [PDF]

				J. D. Furlow, H. Y. Yang, M. Hsu, W. Lim, D. J. Ermio, G. Chiellini, and T. S. Scanlan Induction of Larval Tissue Resorption in Xenopus laevis Tadpoles by the Thyroid Hormone Receptor Agonist GC-1 J. Biol. Chem., June 18, 2004; 279(25): 26555 - 26562. [Abstract] [Full Text] [PDF]

				A. Tomita, D. R. Buchholz, and Y.-B. Shi Recruitment of N-CoR/SMRT-TBLR1 Corepressor Complex by Unliganded Thyroid Hormone Receptor for Gene Repression during Frog Development Mol. Cell. Biol., April 15, 2004; 24(8): 3337 - 3346. [Abstract] [Full Text] [PDF]

				C. C. Helbing, K. Werry, D. Crump, D. Domanski, N. Veldhoen, and C. M. Bailey Expression Profiles of Novel Thyroid Hormone-Responsive Genes and Proteins in the Tail of Xenopus laevis Tadpoles Undergoing Precocious Metamorphosis Mol. Endocrinol., July 1, 2003; 17(7): 1395 - 1409. [Abstract] [Full Text] [PDF]

				L. M. Sachs, P. L. Jones, E. Havis, N. Rouse, B. A. Demeneix, and Y.-B. Shi Nuclear Receptor Corepressor Recruitment by Unliganded Thyroid Hormone Receptor in Gene Repression during Xenopus laevis Development Mol. Cell. Biol., December 15, 2002; 22(24): 8527 - 8538. [Abstract] [Full Text] [PDF]

				K. A. Moutou, A. V. M. Canario, Z. Mamuris, and D. M. Power Molecular cloning and sequence of Sparus aurata skeletal myosin light chains expressed in white muscle: developmental expression and thyroid regulation J. Exp. Biol., January 9, 2001; 204(17): 3009 - 3018. [Abstract] [Full Text] [PDF]

				J. D. Furlow and D. D. Brown In Vitro and in Vivo Analysis of the Regulation of a Transcription Factor Gene by Thyroid Hormone during Xenopus laevis Metamorphosis Mol. Endocrinol., December 1, 1999; 13(12): 2076 - 2089. [Abstract] [Full Text]

				J. Wong, V. C.-T. Liang, L. M. Sachs, and Y.-B. Shi Transcription from the Thyroid Hormone-dependent Promoter of the Xenopus laevis Thyroid Hormone Receptor beta A Gene Requires a Novel Upstream Element and the Initiator, but Not a TATA Box J. Biol. Chem., June 5, 1998; 273(23): 14186 - 14193. [Abstract] [Full Text] [PDF]

				G. M. Wahlström and B. Vennström Requirements for Repression of Retinoid X Receptor by the Oncoprotein P75gag-v-erbA and the Thyroid Hormone Receptors Mol. Endocrinol., May 1, 1998; 12(5): 645 - 653. [Abstract] [Full Text]

				C. D. Hegstrom, L. M. Riddiford, and J. W. Truman Steroid and Neuronal Regulation of Ecdysone Receptor Expression during Metamorphosis of Muscle in the Moth, Manduca sexta J. Neurosci., March 1, 1998; 18(5): 1786 - 1794. [Abstract] [Full Text] [PDF]

				H. T. Jansen, L. S. Lubbers, E. Macchia, L. J. DeGroot, and M. N. Lehman Thyroid Hormone Receptor ({alpha}) Distribution in Hamster and Sheep Brain: Colocalization in Gonadotropin-Releasing Hormone and Other Identified Neurons Endocrinology, November 1, 1997; 138(11): 5039 - 5047. [Abstract] [Full Text] [PDF]

				R. J. Denver, S. Pavgi, and Y.-B. Shi Thyroid Hormone-dependent Gene Expression Program for Xenopus Neural Development J. Biol. Chem., March 28, 1997; 272(13): 8179 - 8188. [Abstract] [Full Text] [PDF]

				M. Puzianowska-Kuznicka, J. Wong, A. Kanamori, and Y.-B. Shi Functional Characterization of a Mutant Thyroid Hormone Receptor in Xenopus laevis J. Biol. Chem., December 27, 1996; 271(52): 33394 - 33403. [Abstract] [Full Text] [PDF]

				J Wong, Y B Shi, and A P Wolffe A role for nucleosome assembly in both silencing and activation of the Xenopus TR beta A gene by the thyroid hormone receptor. Genes & Dev., November 1, 1995; 9(21): 2696 - 2711. [Abstract] [PDF]

				J. Wong and Y.-B. Shi Coordinated Regulation of and Transcriptional Activation by Xenopus Thyroid Hormone and Retinoid X Receptors J. Biol. Chem., August 4, 1995; 270(31): 18479 - 18483. [Abstract] [Full Text] [PDF]

				F. Lezoualc'h, I. Seugnet, A. L. Monnier, J. Ghysdael, J.-P. Behr, and B. A. Demeneix Inhibition of Neurogenic Precursor Proliferation by Antisense [IMAGE] Thyroid Hormone Receptor Oligonucleotides J. Biol. Chem., May 19, 1995; 270(20): 12100 - 12108. [Abstract] [Full Text] [PDF]

				J. Truman, W. Talbot, S. Fahrbach, and D. Hogness Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development Development, January 1, 1994; 120(1): 219 - 234. [Abstract] [PDF]

				E. M. Callery and R. P. Elinson From the Cover: Thyroid hormone-dependent metamorphosis in a direct developing frog PNAS, March 14, 2000; 97(6): 2615 - 2620. [Abstract] [Full Text] [PDF]