How Hormones Regulate Programmed Cell Death during Amphibian Metamorphosis

  • Jamshed R. Tata

Abstract

Extensive programmed cell death is initiated at the onset of amphibian metamorphosis, resulting in 100% of cells dying in some larval tissues, as during total regression of tail and gills. All cell death during metamorphosis is under the control of thyroid hormone (TH), which can initiate the process precociously in whole tadpoles, or in individual tissues in culture. The hormone prolactin (PRL), given exogenously, prevents natural and TH-induced metamorphosis. We have exploited this dual hormonal regulation in premetamorphic Xenopus tails in organ culture to identify and characterize “early” genes that are TH-induced and considered important for initiating cell death. Among the earliest genes activated by TH is that encoding the thyroid hormone receptor TRβ. This autoinduction of TR genes is considered important since, in blocking this process, PRL also inhibited the expression of other TH-inducible genes and prevented cell death. The expression of “early” genes other than TR genes, that are known to promote cell death (e.g. nur-77 and ICE) or survival (e.g. Xenopus bcl-2-like genes), is also considered to be important for the initiation of programmed cell death during amphibian metamorphosis. The possible significance of thyroid hormone-mediated amphibian metamorphosis to mammalian fetal development will be briefly discussed.

Keywords

Thyroid Hormone Thyroid Hormone Receptor Xenopus Tadpole Amphibian Metamorphosis Tadpole Tail 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Atkinson, B.G. 1981. Biological basis of tissue regression and synthesis. In Metamorphosis. Edited by L.I. Gilbert and E. Frieden. Plenum Press, New York. pp. 397–444.CrossRefGoogle Scholar
  2. Baker, B.S. and Tata, J.R. 1992. Prolactin prevents the autoinduction of thyroid hormone receptor mRNAs during amphibian metamorphosis. Dev. Biol. 149, 463–467.PubMedCrossRefGoogle Scholar
  3. Beckingham Smith, K. and Tata, J.R. 1976a. The hormonal control of amphibian metamorphosis. In “Developmental Biology of Plants and Animals”. Edited by C. Graham and P.F. Wareing. Blackwell, Oxford, pp. 232–245.Google Scholar
  4. Beckingham Smith, K. and Tata, J.R. 1976b. Cell death. Are new proteins synthesised during hormone-induced tadpole tail regression? Exp. Cell Res. 100, 129–146.CrossRefGoogle Scholar
  5. Boise, L.H., Gonzáles-Garcia, M., Postema, C.E., Ding, L., Lindsten, T., Turka, L.A., Mao, X., Nunez, G. and Thompson, C.B. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 7A, 597.CrossRefGoogle Scholar
  6. Brown, D.D., Wang, Z., Furlow, J.D., Kanamori, A., Schwartzman, R.A., Remo, B.F. and Pinder, A. 1996. The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis. Proc. Natl. Acad. Sci. USA 93, 1924–1929.PubMedCrossRefGoogle Scholar
  7. Chatterjee, V.K.K. and Tata, J.R. 1992. Thyroid hormone receptors and their role in development. Cancer Surveys 14, 147–167.PubMedGoogle Scholar
  8. Cruz-Reyes, J. and Tata, J.R. 1995. Cloning, characterization and expression of two Xenopus bcl-2-like cell-survival genes. Gene 158, 171–179.PubMedCrossRefGoogle Scholar
  9. Dexter, T.M., Raff, M.C. and Wyllie, A.H. (eds.) 1994. Death from inside out: the role of apoptosis in development, tissue homeostasis and malignancy. Phil. Trans Roy. Soc. B, Vol. 345.Google Scholar
  10. Eliceiri, B. and Brown, D.D. 1994. Quantitation of endogenous thyroid hormone receptor a and β during embryogenesis and metamorphosis inXenopus laevis. J. Biol. Chem. 269, 24459–24465.PubMedGoogle Scholar
  11. Ellis, R.E., Yuan, J. and Horvitz, H.R. 1991. Mechanisms and functions of cell death. Ann. Rev. Cell Biol. 7, 663–698.PubMedCrossRefGoogle Scholar
  12. Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science 240, 889–895.PubMedCrossRefGoogle Scholar
  13. Galton, V.A. 1990. Mechanisms underlying the acceleration of thyroid hormone-induced tadpole metamorphosis by corticosterone. Endocrinology 127, 2997–3002.PubMedCrossRefGoogle Scholar
  14. Gilbert, L.I. and Frieden, E. (eds.) 1981. “Metamorphosis: A problem in developmental biology”. Plenum Press, New York.Google Scholar
  15. Gilbert, L.I., Tata, J.R. and Atkinson, B.G. (eds.) 1996. “Metamorphosis”. Academic Press, San Diego.Google Scholar
  16. Ishizuya-Oka, A. and Shimozawa, A. 1991. Induction of metamorphosis by thyroid hormone in anuran small intestine cultured organotypically in vitro. In Vitro Cell. Dev. Biol. 27A, 853–857.PubMedCrossRefGoogle Scholar
  17. Ishizuya-Oka, A. and Shimozawa, A. 1992. Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivo and in vitro. J. Morphol. 213, 185–195.PubMedCrossRefGoogle Scholar
  18. Iwamuro, S. and Tata, J.R. 1995. Contrasting patterns of expression of thyroid hormone and retinoid X receptor genes during hormonal manipulation of Xenopus tadpole tail regression in culture. Mol. Cell. Endocrinol. 113, 235–243.PubMedCrossRefGoogle Scholar
  19. Kanamori, A. and Brown, D.D. 1993. Cultured cells as a model for amphibian metamorphosis. Proc. Natl. Acad. Sci. USA 90, 6013–6017.PubMedCrossRefGoogle Scholar
  20. Kawahara, A., Baker, B. and Tata, J.R. 1991. Developmental and regional expression of thyroid hormone receptor genes during Xenopus metamorphosis. Development 112, 933–943.PubMedGoogle Scholar
  21. Kikuyama, S., Kawamura, K., Tanaka, S. and Yamamoto, K. 1993. Aspects of amphibian metamorphosis. Hormonal control. Int. Rev. Cytol. 145, 105–148.PubMedCrossRefGoogle Scholar
  22. Kollros, J.J. 1981. Transitions in the nervous system during amphibian metamorphosis. In Metamorphosis. Edited by L.I. Gilbert and E. Frieden. Plenum Press, New York. pp. 445–459.CrossRefGoogle Scholar
  23. Korsmeyer, S.J. 1992. Bcl-2 initiates a new category of oncogenes, Regulators of cell death. Blood 80, 879–886.PubMedGoogle Scholar
  24. Lavin, M. and Watters, D. (eds.) 1993. The cellular and molecular biology of apoptosis. Harwood Academic Publishers, Chur.Google Scholar
  25. Leloup, J. and Buscaglia, M. 1977. La triiodothyronine, hormone de la metamorphose des amphibiens. C.R. Acad. Sci. 284, 2261–2263.Google Scholar
  26. Lockshin, R.A. 1981. Cell death in metamorphosis. In Cell death in biology and pathology. Edited by I.D. Bowen and R.A. Lockshin. Chapman and Hall, London, pp. 79–121.CrossRefGoogle Scholar
  27. Machuca, I. and Tata, J.R. 1992. Autoinduction of thyroid hormone receptor during metamorphosis is reproduced in Xenopus XTC-2 cells. Molec. Cell. Endocr. 87, 105–113.PubMedCrossRefGoogle Scholar
  28. Machuca, I., Esslemont, G., Fairclough, L. and Tata, J.R. 1995. Analysis of structure and expression of the Xenopus thyroid hormone receptor β (xTRβ) gene to explain its autoinduction. Molec. Endocrinol. 9, 96–107.CrossRefGoogle Scholar
  29. Mangelsdorf, D.J. and Evans, R.M. 1995. The RXR heterodimers and orphan receptors. Cell 83, 841–850.PubMedCrossRefGoogle Scholar
  30. Rabelo, E.M.L., Baker, B. and Tata, J.R. 1994. Interplay between thyroid hormone and estrogen in modulating expression of their receptor and vitellogenin genes during Xenopus metamorphosis. Mech. Develop. 45, 49–57.CrossRefGoogle Scholar
  31. Ranjan, M., Wong, J. and Shi, Y.-B. 1994. Transcriptional repression of Xenopus TRβ gene is mediated by a thyroid hormone response element located near the start site. J. Biol. Chem. 269, 24699–24705.PubMedGoogle Scholar
  32. Ray, L.B. and Dent, J.N. 1986. Observations on the interaction of prolactin and thyroxine in the tail of the bullfrog tadpole. Gen. Comp. Endocrinol. 64, 36–43.PubMedCrossRefGoogle Scholar
  33. Rillema, J.A. (ed.) 1987. Actions of prolactin on molecular processes”. Boca Raton, FL, CRC Press.Google Scholar
  34. Rui, H., Lebrun, J.-J., Kirken, R.A., Kelly, P.A. and Farrar, W.L. 1994. JAK2 Activation and cell proliferation induced by antibody-mediated prolactin receptor dimerization. Endocrinology 135, 1299–1306.PubMedCrossRefGoogle Scholar
  35. Shi, Y.-B. 1996. Thyroid hormone-regulated early and late genes during amphibian metamorphosis. In: “Metamorphosis” (Gilbert, L.I., Tata, J.R. and Atkinson, B.G., eds.) pp. 505-538.Google Scholar
  36. Shi, Y.-B. and Brown, D.D. 1993. The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J. Biol. Chem. 268, 20, 312–20, 317.Google Scholar
  37. Shi, Y.-B. and Ishizuya-Oka, A. 1996. Biphasic intestinal development in amphibians. Embryogenesis and remodeling during metamorphosis. Curr. Topics in Dev. Biol. 32, 205–235.CrossRefGoogle Scholar
  38. Tata, J.R. 1966. Requirement for RNA protein synthesis for induced regression of the tadpole tail in organ culture. Dev. Biol. 13, 77–94.PubMedCrossRefGoogle Scholar
  39. Tata, J.R. 1968. Early metamorphic competence of Xenopus larvae. Dev. Biol. 18, 415–440.PubMedCrossRefGoogle Scholar
  40. Tata, J.R. 1971. Protein synthesis during amphibian metamorphosis. Current Topics Dev. Biol. 6, 79–110.CrossRefGoogle Scholar
  41. Tata, J.R. 1993. Gene expression during metamorphosis: An ideal model for post-embryonic development. BioEssays 15, 239–248.PubMedCrossRefGoogle Scholar
  42. Tata, J.R. 1994. Hormonal regulation of programmed cell death during amphibian metamorphosis. Biochem. Cell Biol. 72, 581–588.PubMedCrossRefGoogle Scholar
  43. Tata, J.R. 1996. Hormonal interplay and thyroid hormone receptor expression during amphibian metamorphosis. In “Metamorphosis” (Gilbert, L.I., Tata, J.R. and Atkinson, B.G. eds.) pp. 466–503. Academic Press, San Diego.Google Scholar
  44. Tata, J.R., Kawahara, A. and Baker, B.S. 1991. Prolactin inhibits both thyroid hormone-induced morphogenesis and cell death in cultured amphibian larval tissues. Dev. Biol. 146, 72–80.PubMedCrossRefGoogle Scholar
  45. Tata, J.R., Baker, B.S., Machuca, I., Rabelo, E.M.L. and Yamauchi, K. 1993. Autoinduction of nuclear receptor genes and its significance. J. Steroid Biochem. Molec. Biol. 46, 105–119.PubMedCrossRefGoogle Scholar
  46. Tomei, L.D. and Cope, F.O. (eds.) 1991. The molecular basis of cell death. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.Google Scholar
  47. Ulisse, S., Esslemont, G., Baker, B.S., Chatterjee, V.K.K. and Tata, J.R. 1996. Dominant-negative mutant thyroid hormone receptors prevent transcription from Xenopus thyroid hormone receptor β gene promoter in response to thyroid hormone in Xenopus tadpoles in vivo. Proc. Natl. Acad. Sci. USA 93, 1205–1209.PubMedCrossRefGoogle Scholar
  48. Wang, Z. and Brown, D.D. 1993. Thyroid hormone-induced gene expression program for amphibian tail resorption. J. Biol. Chem. 268, 16, 270-16, 278.Google Scholar
  49. Weber, R. 1965. Inhibitory effect of actinomycin on tail atrophy in Xenopus larvae at metamorphosis. Experientia 21, 665–666.PubMedCrossRefGoogle Scholar
  50. Weber, R. 1969. Tissue involution and lysosomal enzymes during anuran metamorphosis. In Lysosomes in biology and pathology. Edited by J.T. Dingle and H.B. Fell. Vol. I. North-Holland, Amsterdam, pp. 437–461.Google Scholar
  51. Weite, T., Garimorth, K., Philipp, S. and Doppler, W. 1994. Prolactin-dependent activation of a tyrosine phosphorylated DNA binding factor in mouse mammary epithelial cells. Molec. Endocrinol. 8, 1091–1102.CrossRefGoogle Scholar
  52. White, B.A. and Nicoll, C.S. 1981. Hormonal control of amphibian metamorphosis. In Metamorphosis. A problem in developmental biology. Edited by L.I. Gilbert and E. Frieden. Plenum Press, New York. pp. 363–396.CrossRefGoogle Scholar
  53. Wong, J. and Shi, Y.-B. 1995. Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J. Biol. Chem. 270, 18479–18483.PubMedCrossRefGoogle Scholar
  54. Yaoita, Y. and Brown, D.D. 1990. A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis. Genes & Dev. 4, 1917–1924.CrossRefGoogle Scholar
  55. Yoshizato, K. 1989. Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int. Rev. Cytol. 119, 97–149.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Jamshed R. Tata
    • 1
  1. 1.National Institute for Medical ResearchLondonUK

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