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Role of Thyroid Hormone Receptor in Amphibian Development

  • Liezhen Fu
  • Luan Wen
  • Yun-Bo Shi
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1801)

Abstract

The amphibian Xenopus laevis has long been used as a model for studying vertebrate cell and developmental biology largely due to the easiness to manipulate this system in vivo and in vitro. While most of the developmental studies have been on Xenopus embryogenesis, considerable efforts have been made to understand its metamorphosis, a process mimicking postembryonic development in mammals when many organs mature into their adult forms in the presence of high levels of thyroid hormone (T3). Amphibian metamorphosis is totally dependent on T3 and offers a number of advantages for experimental analyses compared to the late stage, uterus-enclosed mammalian embryos. Earlier studies on metamorphosis in Xenopus laevis have revealed dual functions of T3 receptors (TR) during premetamorphic development and metamorphosis as well as important roles of TR-interacting corepressors and coactivators during these two periods, respectively. The development of gene-editing technologies that functions in amphibians in recent years has made possible for the first time to study function of endogenous TRs, especially in the highly related diploid anuran species Xenopus tropicalis. Here, we first review the current mechanistic understanding of the regulation of metamorphosis by T3 and TR, and then describe a detailed method to use TALEN to knock out TRα for studying its role in gene regulation by T3 in vivo and Xenopus development.

Key words

Xenopus laevis Xenopus tropicalis Metamorphosis Gene-editing Thyroid hormone receptor Postembryonic development TALEN 

Notes

Acknowledgments

This work in the laboratory was supported by the Intramural Research Program of National Institute of Child Health and Human Development, National Institutes of Health.

References

  1. 1.
    Shi Y-B (1999) Amphibian metamorphosis: from morphology to molecular biology. John Wiley & Sons, Inc., New YorkGoogle Scholar
  2. 2.
    Tata JR (1993) Gene expression during metamorphosis: an ideal model for post-embryonic development. BioEssays 15(4):239–248CrossRefPubMedGoogle Scholar
  3. 3.
    Lazar MA (1993) Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 14(2):184–193PubMedGoogle Scholar
  4. 4.
    Evans RM (1988) The steroid and thyroid hormone receptor superfamily. Science 240:889–895CrossRefPubMedGoogle Scholar
  5. 5.
    Yen PM (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81(3):1097–1142CrossRefPubMedGoogle Scholar
  6. 6.
    Davis PJ, Davis FB (1996) Nongenomic actions of thyroid hormone. Thyroid 6:497–504CrossRefPubMedGoogle Scholar
  7. 7.
    Tsai MJ, O'Malley BW (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451–486CrossRefPubMedGoogle Scholar
  8. 8.
    Buchholz DR, Paul BD, Fu L, Shi YB (2006) Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol 145(1):1–19CrossRefPubMedGoogle Scholar
  9. 9.
    Davis PJ, Davis FB, Cody V (2005) Membrane receptors mediating thyroid hormone action. Trends Endocrinol Metab 16(9):429–435CrossRefPubMedGoogle Scholar
  10. 10.
    Shi YB, Matsuura K, Fujimoto K, Wen L, Fu L (2012) Thyroid hormone receptor actions on transcription in amphibia: the roles of histone modification and chromatin disruption. Cell Biosci 2(1):42.  https://doi.org/10.1186/2045-3701-2-42. 2045-3701-2-42 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Guigon CJ, Cheng SY (2009) Novel non-genomic signaling of thyroid hormone receptors in thyroid carcinogenesis. Mol Cell Endocrinol 308(1–2):63–69CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hiroi Y, Kim HH, Ying H, Furuya F, Huang Z, Simoncini T, Noma K, Ueki K, Nguyen NH, Scanlan TS, Moskowitz MA, Cheng SY, Liao JK (2006) Rapid nongenomic actions of thyroid hormone. Proc Natl Acad Sci U S A 103(38):14104–14109CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Yaoita Y, Brown DD (1990) A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis. Genes Dev 4(11):1917–1924CrossRefPubMedGoogle Scholar
  14. 14.
    Wong J, Shi Y-B (1995) Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J Biol Chem 270:18479–18483CrossRefPubMedGoogle Scholar
  15. 15.
    Wang X, Matsuda H, Shi Y-B (2008) Developmental regulation and function of thyroid hormone receptors and 9-cis retinoic acid receptors during Xenopus tropicalis metamorphosis. Endocrinology 149:5610–5618CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Leloup J, Buscaglia M (1977) La triiodothyronine: hormone de la métamorphose des amphibiens. CR Acad Sci 284:2261–2263Google Scholar
  17. 17.
    Shi Y-B, Wong J, Puzianowska-Kuznicka M, Stolow M (1996) Tadpole competence and tissue-specific temporal regulation of amphibian metamorphosis: roles of thyroid hormone and its receptors. BioEssays 18:391–399CrossRefPubMedGoogle Scholar
  18. 18.
    Sachs LM, Damjanovski S, Jones PL, Li Q, Amano T, Ueda S, Shi YB, Ishizuya-Oka A (2000) Dual functions of thyroid hormone receptors during Xenopus development. Comp Biochem Physiol B Biochem Mol Biol 126(2):199–211CrossRefPubMedGoogle Scholar
  19. 19.
    Puzianowska-Kuznicka M, Damjanovski S, Shi Y-B (1997) Both thyroid hormone and 9-cis retinoic acid receptors are required to efficiently mediate the effects of thyroid hormone on embryonic development and specific gene regulation in xenopus laevis. Mol Cell Biol 17:4738–4749CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Amaya E, Kroll KL (1999) A method for generating transgenic frog embryos. Methods Mol Biol 97:393–414PubMedGoogle Scholar
  21. 21.
    Nakajima K, Yaoita Y (2003) Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn 227:246–255CrossRefPubMedGoogle Scholar
  22. 22.
    Schreiber AM, Brown DD (2003) Tadpole skin dies autonomously in response to thyroid hormone at metamorphosis. Proc Natl Acad Sci U S A 100:1769–1774CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Das B, Schreiber AM, Huang H, Brown DD (2002) Multiple thyroid hormone-induced muscle growth and death programs during metamorphosis in Xenopus laevis. Proc Natl Acad Sci U S A 99:12230–12235CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Schreiber AM, Das B, Huang H, Marsh-Armstrong N, Brown DD (2001) Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. Proc Natl Acad Sci U S A 98:10739–10744CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Buchholz DR, Hsia VS-C, Fu L, Shi Y-B (2003) A dominant negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Mol Cell Biol 23:6750–6758CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Buchholz DR, Tomita A, Fu L, Paul BD, Shi Y-B (2004) Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Mol Cell Biol 24:9026–9037CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Hasebe T, Buchholz DR, Shi YB, Ishizuya-Oka A (2011) Epithelial-connective tissue interactions induced by thyroid hormone receptor are essential for adult stem cell development in the Xenopus laevis intestine. Stem Cells 29(1):154–161.  https://doi.org/10.1002/stem.560 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Guo X, Zhang T, Hu Z, Zhang Y, Shi Z, Wang Q, Cui Y, Wang F, Zhao H, Chen Y (2014) Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development 141(3):707–714.  https://doi.org/10.1242/dev.099853 CrossRefPubMedGoogle Scholar
  29. 29.
    Lei Y, Guo X, Deng Y, Chen Y, Zhao H (2013) Generation of gene disruptions by transcription activator-like effector nucleases (TALENs) in Xenopus tropicalis embryos. Cell Biosci 3(1):21.  https://doi.org/10.1186/2045-3701-3-21. 2045-3701-3-21 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lei Y, Guo X, Liu Y, Cao Y, Deng Y, Chen X, Cheng CH, Dawid IB, Chen Y, Zhao H (2012) Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci U S A 109:17484–17489.  https://doi.org/10.1073/pnas.1215421109. 1215421109 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Nakayama T, Fish MB, Fisher M, Oomen-Hajagos J, Thomsen GH, Grainger RM (2013) Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis. Genesis 51(12):835–843.  https://doi.org/10.1002/dvg.22720 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Blitz IL, Biesinger J, Xie X, Cho KW (2013) Biallelic genome modification in F(0) Xenopus tropicalis embryos using the CRISPR/Cas system. Genesis 51(12):827–834.  https://doi.org/10.1002/dvg.22719 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wang F, Shi Z, Cui Y, Guo X, Shi YB, Chen Y (2015) Targeted gene disruption in Xenopus laevis using CRISPR/Cas9. Cell Biosci 5:15.  https://doi.org/10.1186/s13578-015-0006-1 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yen PM (2015) Unliganded TRs regulate growth and developmental timing during early embryogenesis: evidence for a dual function mechanism of TR action. Cell Biosci 5:8.  https://doi.org/10.1186/2045-3701-5-8 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Wen L, Shi YB (2015) Unliganded thyroid hormone receptor alpha controls developmental timing in Xenopus tropicalis. Endocrinology 156:721–734.  https://doi.org/10.1210/en.2014-1439 CrossRefPubMedGoogle Scholar
  36. 36.
    Choi J, Suzuki KI, Sakuma T, Shewade L, Yamamoto T, Buchholz DR (2015) Unliganded thyroid hormone receptor alpha regulates developmental timing via gene repression as revealed by gene disruption in Xenopus tropicalis. Endocrinology 156:735–744.  https://doi.org/10.1210/en.2014-1554 CrossRefPubMedGoogle Scholar
  37. 37.
    Sachs LM (2015) Unliganded thyroid hormone receptor function: amphibian metamorphosis got TALENs. Endocrinology 156(2):409–410.  https://doi.org/10.1210/en.2014-2016 CrossRefPubMedGoogle Scholar
  38. 38.
    Wen L, Shibata Y, Su D, Fu L, Luu N, Shi Y-B (2017) Thyroid hormone receptor α controls developmental timing and regulates the rate and coordination of tissue specific metamorphosis in Xenopus tropicalis. Endocrinology 158(6):1985–1998 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Choi J, Ishizuya-Oka A, Buchholz DR (2017) Growth, development, and intestinal remodeling occurs in the absence of thyroid hormone receptor alpha in tadpoles of Xenopus tropicalis. Endocrinology 158(6):1623–1633CrossRefPubMedGoogle Scholar
  40. 40.
    Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39:e82CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Fu L, Buchholz D, Shi YB (2002) Novel double promoter approach for identification of transgenic animals: a tool for in vivo analysis of gene function and development of gene-based therapies. Mol Reprod Dev 62(4):470–476CrossRefPubMedGoogle Scholar
  42. 42.
    Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC (2011) Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 8(1):74–79.  https://doi.org/10.1038/nmeth.1539 CrossRefPubMedGoogle Scholar
  43. 43.
    Wen L, Fu L, Guo X, Chen Y, Shi YB (2015) Histone methyltransferase Dot1L plays a role in postembryonic development in Xenopus tropicalis. FASEB J 29:385–393.  https://doi.org/10.1096/fj.14-252171 CrossRefPubMedGoogle Scholar
  44. 44.
    Vize PD, Melton DA, hemmati-Brivanlou A, Harland RM (1991) Assays for gene function in developing Xenopus embryos. Methods Cell Biol 36:367–387CrossRefPubMedGoogle Scholar
  45. 45.
    Wu M, Gerhart J (1991) Raising Xenopus in the laboratory. Methods Cell Biol 36:3–18CrossRefPubMedGoogle Scholar
  46. 46.
    Qiu P, Shandilya H, D'Alessio JM, O'Connor K, Durocher J, Gerard GF (2004) Mutation detection using surveyor nuclease. BioTechniques 36(4):702–707CrossRefPubMedGoogle Scholar
  47. 47.
    Vouillot L, Thelie A, Pollet N (2015) Comparison of T7E1 and surveyor mismatch cleavage assays to detect mutations triggered by engineered nucleases. G3 (Bethesda) 5(3):407–415.  https://doi.org/10.1534/g3.114.015834 CrossRefPubMedCentralGoogle Scholar
  48. 48.
    Dahlem TJ, Hoshijima K, Jurynec MJ, Gunther D, Starker CG, Locke AS, Weis AM, Voytas DF, Grunwald DJ (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet 8(8):e1002861.  https://doi.org/10.1371/journal.pgen.1002861 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Sedlak RH, Liang S, Niyonzima N, De Silva Feelixge HS, Roychoudhury P, Greninger AL, Weber ND, Boissel S, Scharenberg AM, Cheng A, Magaret A, Bumgarner R, Stone D, Jerome KR (2016) Digital detection of endonuclease mediated gene disruption in the HIV provirus. Sci Rep 6:20064.  https://doi.org/10.1038/srep20064 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Hisano Y, Ota S, Arakawa K, Muraki M, Kono N, Oshita K, Sakuma T, Tomita M, Yamamoto T, Okada Y, Kawahara A (2013) Quantitative assay for TALEN activity at endogenous genomic loci. Biol Open 2(4):363–367.  https://doi.org/10.1242/bio.20133871 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Fu L, Wen L, Luu N, Shi YB (2016) A simple and efficient method to visualize and quantify the efficiency of chromosomal mutations from genome editing. Sci Rep 6:35488.  https://doi.org/10.1038/srep35488 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Section on Molecular MorphogenesisEunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH)BethesdaUSA

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