Abstract
The complex transformation of a tadpole to a frog during amphibian development is under the control of thyroid hormone (T3). T3 is known to regulate gene transcription through its nuclear receptors. We have previously isolated many genes which are up-regulated by T3 in the intestine of Xenopus laevis tadpoles. We have now cloned a full-length cDNA for one such gene (IU12). Sequence analysis shows that the IU12 cDNA encodes a plasma membrane protein with 12 transmembrane domains and homologous to a mammalian gene associated with cell activation and organ development. Similarly, we have found that IU12 is activated during intestinal remodeling when both cell death and proliferation take place. Furthermore, IU12 is an early T3-response gene and its expression in the intestine during T3-induced metamorphosis mimics that during normal development. These results argue for a role of IU12 in the signal transduction pathways leading to intestinal metamorphosis.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Accession codes
References
Atkinson BG . Metamorphosis: Model systems for studying gene expression in postembryonic development. Developmental Genet 1994; 15:313–9.
Shi Y-B . Molecular biology of amphibian metamorphosis: A new approach to an old problem. Trends Endocrinol Metab 1994; 5:14–20.
Tata JR . Gene expression during metamorphosis: An ideal model for post-embryonic development. BioEssays 1993; 15:239–48.
Dodd MHI, Dodd JM . The biology of metamorphosis. In physiology of the amphibia(ed. B.Lofts), pp. 467–599. Academic Press, New York. 1976.
Gilbert LI, Frieden E . Metamorphosis: A problem in developmental biology, 2nd ed., Plenum Press, New York. 1981.
Shi Y-B, Ishizuya-Oka A . Biphasic intestinal development in amphibians: Embryogensis and remodeling during metamorphosis. Current Topics in Develop Biol 1996; 32:205–35.
Balls M, Bownes M . Metamorphosis. The Clarendon Press, Oxford, UK. 1985.
Yoshizato K . Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Inst Rev Cytol 1989; 119:97–149.
Galton VA . Thyroid hormone action in amphibian metamorphosis. In Oppenheimer, J.H., Samuels, H.H., eds. Molecular basis of thyroid hormone action. New York, Academic, 1983; pp 445–83.
Kikuyama S, Kawamura K, Tanaka S, Yamamoto K . Aspects of amphibian metamorphosis: hormonal control. Int Rev Cytol 1993; 145:105–48.
Mangelsdorf D J, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM . The nuclear receptor superfamily: The second decade. Cell 1995; 83:835–9.
Sap J, Munoz A, Damm K, Goldberg Y, Ghysdael J, Leutz A, Berg H, Vennstrom B . The C-erb-A protein is a high affinity receptor for thyroid hormone. Nature 1986; 324:635–40.
Shi YB, Wong J, Puzianowska-Kuznicka M . Thyroid hormone receptors: Mechanisms of transcriptional regulation and roles during frog development. J Biomed Sci 1996; 3:307–18.
Tsai M-J, O'Malley BW : Molecular mechanisms of action of steroid/thyroid receptor receptor superfamily members. Ann Rev Biochem 1994; 63:451–86.
Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol D J, Evans RM . The c-erb-A gene encodes a thyroid hormone receptor. Nature 1986; 324:641–6.
Brown DD, Wang Z, Furlow JD, Kanamori A, Schwartzman RA, Remo BF, Pinder A . The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis. PNAS 1996; 93:1924–9.
Gilbert LI, Tata JR, Atkinson BG . Metamorphosis: Post-embryonic reprogramming of gene expression in amphibian and insect cells. Academic Press, New York 1996.
Shi Y-B, Brown DD . The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J Biol Chem 1993; 266:20312–7.
Patterton D, Hayes WP, Shi Y-B . Transcriptional activation of the matrix metaoproteinase gene stromelysin-3 coincides with thyroid hormone-induced cell death during frog metamorphosis. Dev Biol 1995; 167:252–62.
Nieuwkoop PD, Faber J . Normal table of Xenopus laevis. North Holland Publishing, Amsterdam. 1956.
Kanamori A . Brown DD . The regulation of thyroid hormone receptor b genes by thyroid hormone in Xenopus laevis. J. Biol. Chem. 1992; 267:739–45.
Shi Y-B, Hayes WP . Thyroid hormone-dependent regulation of the intestinal fatty acid-binding protein gene during amphibian metamorphosis. Dev Biol 1994; 161:48–58.
Maniatis T, Fritsch EF, Sambrook J . Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York 1982.
Ranjan M, Wong J, Shi Y-B . Transcriptional repression of Xenopuf TRβ gene is mediated by a thyroid hormone response element located near the start site. The Journal of Biol Chem 1994; 269:24699–705.
Herrin DL, Schmidt GW . Rapid reversible staining of Northern blots prior to hybridization. BioTechniques 1988; 6:196–200.
Shi Y-B, Liang VC-T . Cloning and characterization of the ribosomal protein L8 gene from Xenopus laevis. Biochimica et Biophysica Acta. 1994; 1217:227–8.
Buckbinder L, Brown DD . Thyroid hormone-induced gene expression changes in the developing frog limb. J Biol Chem 1992; 267:25786–91.
Stolow MA, Shi Y-B . Xenopus sonic hedgehog as a potential morphogen during embryogenesis and thyroid hormone-dependent metamorphosis. Nucl Acids Res 1995; 23:2555–62.
Wang Z, Brown DD . Thyroid hormone-induced gene expression program for amphibai tail resorption. J Biol Chem 1993; 268:16270–78.
Ishizuya-Oka A, Stolow MA, Ueda S, Shi Y-B . Temporal and Spatial Expression of An Intestinal Na+/PO43− Cotransporter Correlates With Epithelial Transformation During Thyroid Hormone-Dependent Frog Metamorphosis. Dev Gen 1997; 20:53–66.
Patterton D, Shi Y-B . Thyroid Hormone-dependent Differential Regulation of Multiple Arginase Genes during Amphibian Metamorphosis. J Biol Chem 1994; 269:25328–34.
Von Heijne G . A new method for predicting sigmal sequence cleavage sites. Nucleic Acids Research 1986; 14:4683–90.
Gaugitsch HW, Prieschl EE, Kalthoff F, Huber NE, Baumruker TA . Novel Transiently Expressed, Integral Membrane Protein Linked to Cell Activation. J Biol Chem 1992; 267:11267–73.
Sang J, Lim YP, Panziaca M, Finch P, Thomspon NL . TA1, a highly conserved oncofetal complementary DNA from rat hepatoma, encodes an integral membrane protein associated with liver development, carcinogenesis, and cell activation. Cancer Res 1995; 55:1152–9.
Leloup J, Buscaglia M . La triiodothyronine: hormone de la mtamorphose des amphibiens. CR Acad Sci 1977; 284:2261–3.
Dauca M . Hourdry J . Transformations in the intestinal epithelium during anuran metamorphosis. In Metamorphosis (Balls M. and Bownes, M., eds). pp. 36–58. The clarendon Press, Oxford, UK. 1985.
Ishizuya-Oka A, and Ueda S . Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res 1996; 286:467–76.
Su Y, Shi Y, Shi Y-B . Cyclosporin A but not FK 506 inhibits thyroid hormoneinduced apoptosis in tadpole intestinal epithelium. FASEB J 1997; 11:559–65.
Ishizuya-Oka A, Shimozawa A . Development of the connective tissue in the digestive tract of the larval and metamorphosing Xenopus laevis. Ant Anz Jena 1987; 164:81–93.
McAvoy JW, Dixon KE . Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis. J Exp Zool 1977; 202:129–38.
Acknowledgements
We would like to thank Ms. Kieu Pham for preparing the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liang, V., Sedgwick, T. & Shi, Y. Characterization of the Xenopus homolog of an immediate early gene associated with cell activation: sequence analysis and regulation of its expression by thyroid hormone during amphibian metamorphosis. Cell Res 7, 179–193 (1997). https://doi.org/10.1038/cr.1997.19
Received:
Revised:
Accepted:
Issue date:
DOI: https://doi.org/10.1038/cr.1997.19
