Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1992 Mar;11(3):1003–1013. doi: 10.1002/j.1460-2075.1992.tb05139.x

Evolution of the nuclear receptor gene superfamily.

V Laudet 1, C Hänni 1, J Coll 1, F Catzeflis 1, D Stéhelin 1
PMCID: PMC556541  PMID: 1312460

Abstract

Nuclear receptor genes represent a large family of genes encoding receptors for various hydrophobic ligands such as steroids, vitamin D, retinoic acid and thyroid hormones. This family also contains genes encoding putative receptors for unknown ligands. Nuclear receptor gene products are composed of several domains important for transcriptional activation, DNA binding (C domain), hormone binding and dimerization (E domain). It is not known whether these genes have evolved through gene duplication from a common ancestor or if their different domains came from different independent sources. To test these possibilities we have constructed and compared the phylogenetic trees derived from two different domains of 30 nuclear receptor genes. The tree built from the DNA binding C domain clearly shows a common progeny of all nuclear receptors, which can be grouped into three subfamilies: (i) thyroid hormone and retinoic acid receptors, (ii) orphan receptors and (iii) steroid hormone receptors. The tree constructed from the central part of the E domain which is implicated in transcriptional regulation and dimerization shows the same distribution in three subfamilies but two groups of receptors are in a different position from that in the C domain tree: (i) the Drosophila knirps family genes have acquired very different E domains during evolution, and (ii) the vitamin D and ecdysone receptors, as well as the FTZ-F1 and the NGF1B genes, seem to have DNA binding and hormone binding domains belonging to different classes. These data suggest a complex evolutionary history for nuclear receptor genes in which gene duplication events and swapping between domains of different origins took place.

Full text

PDF
1003

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arriza J. L., Weinberger C., Cerelli G., Glaser T. M., Handelin B. L., Housman D. E., Evans R. M. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science. 1987 Jul 17;237(4812):268–275. doi: 10.1126/science.3037703. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M. Puffs, genes, and hormones revisited. Cell. 1990 Apr 6;61(1):1–3. doi: 10.1016/0092-8674(90)90205-s. [DOI] [PubMed] [Google Scholar]
  3. Baker A. R., McDonnell D. P., Hughes M., Crisp T. M., Mangelsdorf D. J., Haussler M. R., Pike J. W., Shine J., O'Malley B. W. Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc Natl Acad Sci U S A. 1988 May;85(10):3294–3298. doi: 10.1073/pnas.85.10.3294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beato M. Gene regulation by steroid hormones. Cell. 1989 Feb 10;56(3):335–344. doi: 10.1016/0092-8674(89)90237-7. [DOI] [PubMed] [Google Scholar]
  5. Beebe J. S., Darling D. S., Chin W. W. 3,5,3'-triiodothyronine receptor auxiliary protein (TRAP) enhances receptor binding by interactions within the thyroid hormone response element. Mol Endocrinol. 1991 Jan;5(1):85–93. doi: 10.1210/mend-5-1-85. [DOI] [PubMed] [Google Scholar]
  6. Bisbee C. A., Baker M. A., Wilson A. C., Haji-Azimi I., Fischberg M. Albumin phylogeny for clawed frogs (Xenopus). Science. 1977 Feb 25;195(4280):785–787. doi: 10.1126/science.65013. [DOI] [PubMed] [Google Scholar]
  7. Brunt S. A., Riehl R., Silver J. C. Steroid hormone regulation of the Achlya ambisexualis 85-kilodalton heat shock protein, a component of the Achlya steroid receptor complex. Mol Cell Biol. 1990 Jan;10(1):273–281. doi: 10.1128/mcb.10.1.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chang C., Kokontis J., Acakpo-Satchivi L., Liao S., Takeda H., Chang Y. Molecular cloning of new human TR2 receptors: a class of steroid receptor with multiple ligand-binding domains. Biochem Biophys Res Commun. 1989 Dec 15;165(2):735–741. doi: 10.1016/s0006-291x(89)80028-2. [DOI] [PubMed] [Google Scholar]
  9. Chang C., Kokontis J. Identification of a new member of the steroid receptor super-family by cloning and sequence analysis. Biochem Biophys Res Commun. 1988 Sep 15;155(2):971–977. doi: 10.1016/s0006-291x(88)80591-6. [DOI] [PubMed] [Google Scholar]
  10. Damm K., Beug H., Graf T., Vennström B. A single point mutation in erbA restores the erythroid transforming potential of a mutant avian erythroblastosis virus (AEV) defective in both erbA and erbB oncogenes. EMBO J. 1987 Feb;6(2):375–382. doi: 10.1002/j.1460-2075.1987.tb04765.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Darling D. S., Beebe J. S., Burnside J., Winslow E. R., Chin W. W. 3,5,3'-triiodothyronine (T3) receptor-auxiliary protein (TRAP) binds DNA and forms heterodimers with the T3 receptor. Mol Endocrinol. 1991 Jan;5(1):73–84. doi: 10.1210/mend-5-1-73. [DOI] [PubMed] [Google Scholar]
  12. Debuire B., Henry C., Bernissa M., Biserte G., Claverie J. M., Saule S., Martin P., Stehelin D. Sequencing the erbA gene of avian erythroblastosis virus reveals a new type of oncogene. Science. 1984 Jun 29;224(4656):1456–1459. doi: 10.1126/science.6328658. [DOI] [PubMed] [Google Scholar]
  13. Dessen P., Fondrat C., Valencien C., Mugnier C. BISANCE: a French service for access to biomolecular sequence databases. Comput Appl Biosci. 1990 Oct;6(4):355–356. doi: 10.1093/bioinformatics/6.4.355. [DOI] [PubMed] [Google Scholar]
  14. Dibb N. J., Newman A. J. Evidence that introns arose at proto-splice sites. EMBO J. 1989 Jul;8(7):2015–2021. doi: 10.1002/j.1460-2075.1989.tb03609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 1988 May 13;240(4854):889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fawell S. E., Lees J. A., White R., Parker M. G. Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell. 1990 Mar 23;60(6):953–962. doi: 10.1016/0092-8674(90)90343-d. [DOI] [PubMed] [Google Scholar]
  17. Fitch W. M. A non-sequential method for constructing trees and hierarchical classifications. J Mol Evol. 1981;18(1):30–37. doi: 10.1007/BF01733209. [DOI] [PubMed] [Google Scholar]
  18. Forman B. M., Samuels H. H. Interactions among a subfamily of nuclear hormone receptors: the regulatory zipper model. Mol Endocrinol. 1990 Sep;4(9):1293–1301. doi: 10.1210/mend-4-9-1293. [DOI] [PubMed] [Google Scholar]
  19. Forrest D., Sjöberg M., Vennström B. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J. 1990 May;9(5):1519–1528. doi: 10.1002/j.1460-2075.1990.tb08270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Giguère V., Yang N., Segui P., Evans R. M. Identification of a new class of steroid hormone receptors. Nature. 1988 Jan 7;331(6151):91–94. doi: 10.1038/331091a0. [DOI] [PubMed] [Google Scholar]
  21. Glass C. K., Lipkin S. M., Devary O. V., Rosenfeld M. G. Positive and negative regulation of gene transcription by a retinoic acid-thyroid hormone receptor heterodimer. Cell. 1989 Nov 17;59(4):697–708. doi: 10.1016/0092-8674(89)90016-0. [DOI] [PubMed] [Google Scholar]
  22. Green S., Chambon P. Nuclear receptors enhance our understanding of transcription regulation. Trends Genet. 1988 Nov;4(11):309–314. doi: 10.1016/0168-9525(88)90108-4. [DOI] [PubMed] [Google Scholar]
  23. Green S., Kumar V., Theulaz I., Wahli W., Chambon P. The N-terminal DNA-binding 'zinc finger' of the oestrogen and glucocorticoid receptors determines target gene specificity. EMBO J. 1988 Oct;7(10):3037–3044. doi: 10.1002/j.1460-2075.1988.tb03168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Green S., Walter P., Kumar V., Krust A., Bornert J. M., Argos P., Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986 Mar 13;320(6058):134–139. doi: 10.1038/320134a0. [DOI] [PubMed] [Google Scholar]
  25. Hamada K., Gleason S. L., Levi B. Z., Hirschfeld S., Appella E., Ozato K. H-2RIIBP, a member of the nuclear hormone receptor superfamily that binds to both the regulatory element of major histocompatibility class I genes and the estrogen response element. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8289–8293. doi: 10.1073/pnas.86.21.8289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hazel T. G., Nathans D., Lau L. F. A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor superfamily. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8444–8448. doi: 10.1073/pnas.85.22.8444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Henrich V. C., Sliter T. J., Lubahn D. B., MacIntyre A., Gilbert L. I. A steroid/thyroid hormone receptor superfamily member in Drosophila melanogaster that shares extensive sequence similarity with a mammalian homologue. Nucleic Acids Res. 1990 Jul 25;18(14):4143–4148. doi: 10.1093/nar/18.14.4143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  29. Hollenberg S. M., Weinberger C., Ong E. S., Cerelli G., Oro A., Lebo R., Thompson E. B., Rosenfeld M. G., Evans R. M. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature. 1985 Dec 19;318(6047):635–641. doi: 10.1038/318635a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hughes M. R., Malloy P. J., Kieback D. G., Kesterson R. A., Pike J. W., Feldman D., O'Malley B. W. Point mutations in the human vitamin D receptor gene associated with hypocalcemic rickets. Science. 1988 Dec 23;242(4886):1702–1705. doi: 10.1126/science.2849209. [DOI] [PubMed] [Google Scholar]
  31. Insall R., Kay R. R. A specific DIF binding protein in Dictyostelium. EMBO J. 1990 Oct;9(10):3323–3328. doi: 10.1002/j.1460-2075.1990.tb07532.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Issemann I., Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature. 1990 Oct 18;347(6294):645–650. doi: 10.1038/347645a0. [DOI] [PubMed] [Google Scholar]
  33. Koelle M. R., Talbot W. S., Segraves W. A., Bender M. T., Cherbas P., Hogness D. S. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 1991 Oct 4;67(1):59–77. doi: 10.1016/0092-8674(91)90572-g. [DOI] [PubMed] [Google Scholar]
  34. Ladias J. A., Karathanasis S. K. Regulation of the apolipoprotein AI gene by ARP-1, a novel member of the steroid receptor superfamily. Science. 1991 Feb 1;251(4993):561–565. doi: 10.1126/science.1899293. [DOI] [PubMed] [Google Scholar]
  35. Laudet V., Begue A., Henry-Duthoit C., Joubel A., Martin P., Stehelin D., Saule S. Genomic organization of the human thyroid hormone receptor alpha (c-erbA-1) gene. Nucleic Acids Res. 1991 Mar 11;19(5):1105–1112. doi: 10.1093/nar/19.5.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lavorgna G., Ueda H., Clos J., Wu C. FTZ-F1, a steroid hormone receptor-like protein implicated in the activation of fushi tarazu. Science. 1991 May 10;252(5007):848–851. doi: 10.1126/science.1709303. [DOI] [PubMed] [Google Scholar]
  37. Lazar M. A., Hodin R. A., Darling D. S., Chin W. W. A novel member of the thyroid/steroid hormone receptor family is encoded by the opposite strand of the rat c-erbA alpha transcriptional unit. Mol Cell Biol. 1989 Mar;9(3):1128–1136. doi: 10.1128/mcb.9.3.1128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lehmann J. M., Hoffmann B., Pfahl M. Genomic organization of the retinoic acid receptor gamma gene. Nucleic Acids Res. 1991 Feb 11;19(3):573–578. doi: 10.1093/nar/19.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mangelsdorf D. J., Ong E. S., Dyck J. A., Evans R. M. Nuclear receptor that identifies a novel retinoic acid response pathway. Nature. 1990 May 17;345(6272):224–229. doi: 10.1038/345224a0. [DOI] [PubMed] [Google Scholar]
  40. Milbrandt J. Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron. 1988 May;1(3):183–188. doi: 10.1016/0896-6273(88)90138-9. [DOI] [PubMed] [Google Scholar]
  41. Misrahi M., Atger M., d'Auriol L., Loosfelt H., Meriel C., Fridlansky F., Guiochon-Mantel A., Galibert F., Milgrom E. Complete amino acid sequence of the human progesterone receptor deduced from cloned cDNA. Biochem Biophys Res Commun. 1987 Mar 13;143(2):740–748. doi: 10.1016/0006-291x(87)91416-1. [DOI] [PubMed] [Google Scholar]
  42. Miyajima N., Horiuchi R., Shibuya Y., Fukushige S., Matsubara K., Toyoshima K., Yamamoto T. Two erbA homologs encoding proteins with different T3 binding capacities are transcribed from opposite DNA strands of the same genetic locus. Cell. 1989 Apr 7;57(1):31–39. doi: 10.1016/0092-8674(89)90169-4. [DOI] [PubMed] [Google Scholar]
  43. Miyajima N., Kadowaki Y., Fukushige S., Shimizu S., Semba K., Yamanashi Y., Matsubara K., Toyoshima K., Yamamoto T. Identification of two novel members of erbA superfamily by molecular cloning: the gene products of the two are highly related to each other. Nucleic Acids Res. 1988 Dec 9;16(23):11057–11074. doi: 10.1093/nar/16.23.11057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Mlodzik M., Hiromi Y., Weber U., Goodman C. S., Rubin G. M. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell. 1990 Jan 26;60(2):211–224. doi: 10.1016/0092-8674(90)90737-y. [DOI] [PubMed] [Google Scholar]
  45. Moore D. D. Diversity and unity in the nuclear hormone receptors: a terpenoid receptor superfamily. New Biol. 1990 Jan;2(1):100–105. [PubMed] [Google Scholar]
  46. Nauber U., Pankratz M. J., Kienlin A., Seifert E., Klemm U., Jäckle H. Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature. 1988 Dec 1;336(6198):489–492. doi: 10.1038/336489a0. [DOI] [PubMed] [Google Scholar]
  47. Nirde P., Torpier G., De Reggi M. L., Capron A. Ecdysone and 20 hydroxyecdysone: new hormones for the human parasite schistosoma mansoni. FEBS Lett. 1983 Jan 24;151(2):223–227. doi: 10.1016/0014-5793(83)80074-x. [DOI] [PubMed] [Google Scholar]
  48. O'Donnell A. L., Koenig R. J. Mutational analysis identifies a new functional domain of the thyroid hormone receptor. Mol Endocrinol. 1990 May;4(5):715–720. doi: 10.1210/mend-4-5-715. [DOI] [PubMed] [Google Scholar]
  49. O'Donnell A. L., Rosen E. D., Darling D. S., Koenig R. J. Thyroid hormone receptor mutations that interfere with transcriptional activation also interfere with receptor interaction with a nuclear protein. Mol Endocrinol. 1991 Jan;5(1):94–99. doi: 10.1210/mend-5-1-94. [DOI] [PubMed] [Google Scholar]
  50. O'Malley B. W. Did eucaryotic steroid receptors evolve from intracrine gene regulators? Endocrinology. 1989 Sep;125(3):1119–1120. doi: 10.1210/endo-125-3-1119. [DOI] [PubMed] [Google Scholar]
  51. Oro A. E., McKeown M., Evans R. M. Relationship between the product of the Drosophila ultraspiracle locus and the vertebrate retinoid X receptor. Nature. 1990 Sep 20;347(6290):298–301. doi: 10.1038/347298a0. [DOI] [PubMed] [Google Scholar]
  52. Oro A. E., Ong E. S., Margolis J. S., Posakony J. W., McKeown M., Evans R. M. The Drosophila gene knirps-related is a member of the steroid-receptor gene superfamily. Nature. 1988 Dec 1;336(6198):493–496. doi: 10.1038/336493a0. [DOI] [PubMed] [Google Scholar]
  53. Pankratz M. J., Jäckle H. Making stripes in the Drosophila embryo. Trends Genet. 1990 Sep;6(9):287–292. doi: 10.1016/0168-9525(90)90234-w. [DOI] [PubMed] [Google Scholar]
  54. Petkovich M., Brand N. J., Krust A., Chambon P. A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature. 1987 Dec 3;330(6147):444–450. doi: 10.1038/330444a0. [DOI] [PubMed] [Google Scholar]
  55. Pignoni F., Baldarelli R. M., Steingrímsson E., Diaz R. J., Patapoutian A., Merriam J. R., Lengyel J. A. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell. 1990 Jul 13;62(1):151–163. doi: 10.1016/0092-8674(90)90249-e. [DOI] [PubMed] [Google Scholar]
  56. Ponglikitmongkol M., Green S., Chambon P. Genomic organization of the human oestrogen receptor gene. EMBO J. 1988 Nov;7(11):3385–3388. doi: 10.1002/j.1460-2075.1988.tb03211.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ragsdale C. W., Jr, Petkovich M., Gates P. B., Chambon P., Brockes J. P. Identification of a novel retinoic acid receptor in regenerative tissues of the newt. Nature. 1989 Oct 19;341(6243):654–657. doi: 10.1038/341654a0. [DOI] [PubMed] [Google Scholar]
  58. Rothe M., Nauber U., Jäckle H. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 1989 Oct;8(10):3087–3094. doi: 10.1002/j.1460-2075.1989.tb08460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ryseck R. P., Macdonald-Bravo H., Mattéi M. G., Ruppert S., Bravo R. Structure, mapping and expression of a growth factor inducible gene encoding a putative nuclear hormonal binding receptor. EMBO J. 1989 Nov;8(11):3327–3335. doi: 10.1002/j.1460-2075.1989.tb08494.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  61. Sap J., Muñoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986 Dec 18;324(6098):635–640. doi: 10.1038/324635a0. [DOI] [PubMed] [Google Scholar]
  62. Schwabe J. W., Rhodes D. Beyond zinc fingers: steroid hormone receptors have a novel structural motif for DNA recognition. Trends Biochem Sci. 1991 Aug;16(8):291–296. doi: 10.1016/0968-0004(91)90121-b. [DOI] [PubMed] [Google Scholar]
  63. Segraves W. A., Hogness D. S. The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev. 1990 Feb;4(2):204–219. doi: 10.1101/gad.4.2.204. [DOI] [PubMed] [Google Scholar]
  64. Segraves W. A. Something old, some things new: the steroid receptor superfamily in Drosophila. Cell. 1991 Oct 18;67(2):225–228. doi: 10.1016/0092-8674(91)90172-u. [DOI] [PubMed] [Google Scholar]
  65. Shea M. J., King D. L., Conboy M. J., Mariani B. D., Kafatos F. C. Proteins that bind to Drosophila chorion cis-regulatory elements: a new C2H2 zinc finger protein and a C2C2 steroid receptor-like component. Genes Dev. 1990 Jul;4(7):1128–1140. doi: 10.1101/gad.4.7.1128. [DOI] [PubMed] [Google Scholar]
  66. Sladek F. M., Zhong W. M., Lai E., Darnell J. E., Jr Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev. 1990 Dec;4(12B):2353–2365. doi: 10.1101/gad.4.12b.2353. [DOI] [PubMed] [Google Scholar]
  67. Thompson C. C., Weinberger C., Lebo R., Evans R. M. Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system. Science. 1987 Sep 25;237(4822):1610–1614. doi: 10.1126/science.3629259. [DOI] [PubMed] [Google Scholar]
  68. Tilley W. D., Marcelli M., Wilson J. D., McPhaul M. J. Characterization and expression of a cDNA encoding the human androgen receptor. Proc Natl Acad Sci U S A. 1989 Jan;86(1):327–331. doi: 10.1073/pnas.86.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wang L. H., Tsai S. Y., Cook R. G., Beattie W. G., Tsai M. J., O'Malley B. W. COUP transcription factor is a member of the steroid receptor superfamily. Nature. 1989 Jul 13;340(6229):163–166. doi: 10.1038/340163a0. [DOI] [PubMed] [Google Scholar]
  70. Weinberger C., Thompson C. C., Ong E. S., Lebo R., Gruol D. J., Evans R. M. The c-erb-A gene encodes a thyroid hormone receptor. Nature. 1986 Dec 18;324(6098):641–646. doi: 10.1038/324641a0. [DOI] [PubMed] [Google Scholar]
  71. Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Xiong Y., Eickbush T. H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol. 1988 Nov;5(6):675–690. doi: 10.1093/oxfordjournals.molbev.a040521. [DOI] [PubMed] [Google Scholar]
  73. Yaoita Y., Shi Y. B., Brown D. D. Xenopus laevis alpha and beta thyroid hormone receptors. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7090–7094. doi: 10.1073/pnas.87.18.7090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zelent A., Krust A., Petkovich M., Kastner P., Chambon P. Cloning of murine alpha and beta retinoic acid receptors and a novel receptor gamma predominantly expressed in skin. Nature. 1989 Jun 29;339(6227):714–717. doi: 10.1038/339714a0. [DOI] [PubMed] [Google Scholar]
  75. de Thé H., Marchio A., Tiollais P., Dejean A. A novel steroid thyroid hormone receptor-related gene inappropriately expressed in human hepatocellular carcinoma. Nature. 1987 Dec 17;330(6149):667–670. doi: 10.1038/330667a0. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES