Origin and evolution of the ligand-binding ability of nuclear receptors

Molecular and Cellular Endocrinology

Volumn 334, Issue 1-2, 2011, Pages 21-30

  Markov, Gabriel V ^a,b   Laudet, Vincent ^a  

^a University Lyon i   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Comparative endocrinology; Gene duplication; Nuclear receptors; Orthology; Phylogeny

Indexed keywords

AROMATASE; CELL NUCLEUS RECEPTOR; CYTOCHROME P450 3A4; ECDYSONE RECEPTOR; LIVER RECEPTOR HOMOLOG 1; NUCLEUS RECEPTOR 1; NUCLEUS RECEPTOR 3; SEX HORMONE; STEROID RECEPTOR; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

BINDING AFFINITY; CONVERGENT EVOLUTION; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EVOLUTIONARY HOMOLOGY; HORMONE RECEPTOR INTERACTION; HORMONE RESPONSE; LIGAND BINDING; MOLECULAR EVOLUTION; MOLECULAR MODEL; NONHUMAN; PARSIMONY ANALYSIS; PLESIOMORPHY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEROIDOGENESIS; VERTEBRATE; XENOBIOTIC METABOLISM;

EID: 79951671502     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.10.017     Document Type: Review

References (82)

1. Abad P., Gouzy J., Aury J., Castagnone-Sereno P., Danchin E.G.J., Deleury E., Perfus-Barbeoch L., Anthouard V., Artiguenave F., Blok V.C., Caillaud M., Coutinho P.M., Dasilva C., Luca F.D., Deau F., Esquibet M., Flutre T., Goldstone J.V., Hamamouch N., Hewezi T., Jaillon O., Jubin C., Leonetti P., Magliano M., Maier T.R., Markov G.V., McVeigh P., Pesole G., Poulain J., Robinson-Rechavi M., Sallet E., Ségurens B., Steinbach D., Tytgat T., Ugarte E., van Ghelder C., Veronico P., Baum T.J., Blaxter M., Bleve-Zacheo T., Davis E.L., Ewbank J.J., Favery B., Grenier E., Henrissat B., Jones J.T., Laudet V., Maule A.G., Quesneville H., Rosso M., Schiex T., Smant G., Weissenbach J., Wincker P. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 2008, 26:909-915.
2. Amero S.A., Kretsinger R.H., Moncrief N.D., Yamamoto K.R., Pearson W.R. The origin of nuclear receptor proteins: a single precursor distinct from other transcription factors. Mol. Endocrinol. 1992, 6:3-7.
3. Babin P.J., Gibbons G.F. The evolution of plasma cholesterol: direct utility or a " spandrel" of hepatic lipid metabolism?. Prog. Lipid Res. 2009, 48:73-91.
4. Baker M.E. Evolution of 17beta-hydroxysteroid dehydrogenases and their role in androgen, estrogen and retinoid action. Mol. Cell. Endocrinol. 2001, 171:211-215.
5. Baker M.E. Albumin, steroid hormones and the origin of vertebrates. J. Endocrinol. 2002, 175:121-127.
6. Baker M.E. Recent insights into the origins of adrenal and sex steroid receptors. J. Mol. Endocrinol. 2002, 28:149-152.
7. Baker M.E. Evolution of adrenal and sex steroid action in vertebrates: a ligand-based mechanism for complexity. Bioessays 2003, 25:396-400.
8. Baker M.E. Xenobiotics and the evolution of multicellular animals: emergence and diversification of ligand-activated transcription factors. Integr. Comp. Biol. 2005, 45:172-178.
9. Baker M.E. Trichoplax, the simplest known animal, contains an estrogen-related receptor but no estrogen receptor: implications for estrogen receptor evolution. Biochem. Biophys. Res. Commun. 2008, 375:623-627.
10. Bannister R., Beresford N., May D., Routledge E.J., Jobling S., Rand-Weaver M. Novel estrogen receptor-related transcripts in Marisa cornuarietis, a freshwater snail with reported sensitivity to estrogenic chemicals. Environ. Sci. Technol. 2007, 41:2643-2650.
11. Benoit G., Malewicz M., Perlmann T. Digging deep into the pockets of orphan nuclear receptors: insights from structural studies. Trends Cell. Biol. 2004, 14:369-376.
12. Bertrand S., Brunet F.G., Escriva H., Parmentier G., Laudet V., Robinson-Rechavi M. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol. Biol. Evol. 2004, 21:1923-1937.
13. Bridgham J.T., Carroll S.M., Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 2006, 312:97-101.
14. Bridgham J.T., Brown J.E., Rodríguez-Marí A., Catchen J.M., Thornton J.W. Evolution of a new function by degenerative mutation in cephalochordate steroid receptors. PLoS Genet. 2008, 4:e1000191.
15. Brown C.M., Reisfeld B., Mayeno A.N. Cytochromes P450: a structure-based summary of biotransformations using representative substrates. Drug Metab. Rev. 2008, 40:1-100.
16. Burris T.P. Nuclear hormone receptors for heme: REV-ERBalpha and REV-ERBbeta are ligand-regulated components of the mammalian clock. Mol. Endocrinol. 2008, 22:1509-1520.
17. Calléja C., Messaddeq N., Chapellier B., Yang H., Krezel W., Li M., Metzger D., Mascrez B., Ohta K., Kagechika H., Endo Y., Mark M., Ghyselinck N.B., Chambon P. Genetic and pharmacological evidence that a retinoic acid cannot be the RXR-activating ligand in mouse epidermis keratinocytes. Genes Dev. 2006, 20:1525-1538.
18. de Lera A.R., Bourguet W., Altucci L., Gronemeyer H. Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat. Rev. Drug Discov. 2007, 6:811-820.
19. de Rosny E., de Groot A., Jullian-Binard C., Borel F., Suarez C., Pape L.L., Fontecilla-Camps J., Jouve H. DHR51, the Drosophila melanogaster homologue of the human photoreceptor cell-specific nuclear receptor, is a thiolate heme-binding protein. Biochemistry 2008.
20. Durou C., Mouneyrac C. Linking steroid hormone levels to sexual maturity index and energy reserves in Nereis diversicolor from clean and polluted estuaries. Gen. Comp. Endocrinol. 2007, 150:106-113.
21. Eick, G.N., Thornton, J.W., Evolution of steroid receptors from an estrogen-sensitive ancestral protein. Mol. Cell. Endocrinol. doi:10.1016/j.mce.2010.09.003.
22. Ekins S., Reschly E.J., Hagey L.R., Krasowski M.D. Evolution of pharmacologic specificity in the pregnane X receptor. BMC Evol. Biol. 2008, 8:103.
23. Escriva H., Safi R., Hänni C., Langlois M.C., Saumitou-Laprade P., Stehelin D., Capron A., Pierce R., Laudet V. Ligand binding was acquired during evolution of nuclear receptors. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:6803-6808.
24. Escriva H., Delaunay F., Laudet V. Ligand binding and nuclear receptor evolution. Mol. Cell. Endocrinol. 2000, 22:717-727.
25. Escriva H., Bertrand S., Germain P., Robinson-Rechavi M., Umbhauer M., Cartry J., Duffraisse M., Holland L., Gronemeyer H., Laudet V. Neofunctionalization in vertebrates: the example of retinoic acid receptors. PLoS Genet. 2006, 2:e102.
26. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 1988, 240:889-895.
27. Faus H., Haendler B. Post-translational modifications of steroid receptors. Biomed. Pharmacother. 2006, 60:520-528.
28. Germain P., Staels B., Dacquet C., Spedding M., Laudet V. Overview of nomenclature of nuclear receptors. Pharmacol. Rev. 2006, 58:685-704.
29. Giguère V., Yang N., Segui P., Evans R.M. Identification of a new class of steroid hormone receptors. Nature 1988, 331:91-94.
30. Gotoh S., Ohgari Y., Nakamura T., Osumi T., Taketani S. Heme-binding to the nuclear receptor retinoid X receptor alpha (RXRalpha) leads to the inhibition of the transcriptional activity. Gene 2008, 423:207-214.
31. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 2002, 141:131-160.
32. He J., Cheng Q., Xie W. Minireview: Nuclear receptor-controlled steroid hormone synthesis and metabolism. Mol. Endocrinol. 2010, 24:11-21.
33. Henley D.V., Korach K.S. Endocrine-disrupting chemicals use distinct mechanisms of action to modulate endocrine system function. Endocrinology 2006, 147:S25-S32.
34. Heyland A., Hodin J., Reitzel A.M. Hormone signaling in evolution and development: a non-model system approach. Bioessays 2005, 27:64-75.
35. Horner M.A., Pardee K., Liu S., King-Jones K., Lajoie G., Edwards A., Krause H.M., Thummel C.S. The Drosophila DHR96 nuclear receptor binds cholesterol and regulates cholesterol homeostasis. Genes Dev. 2009, 23:2711-2716.
36. Howard-Ashby M., Materna S.C., Brown C.T., Chen L., Cameron R.A., Davidson E.H. Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus. Dev. Biol. 2006, 300:90-107.
37. Huang P., Chandra V., Rastinejad F. Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu. Rev. Physiol. 2010, 72:247-272.
38. Iwema T., Billas I.M.L., Beck Y., Bonneton F., Nierengarten H., Chaumot A., Richards G., Laudet V., Moras D. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. EMBO J. 2007, 26:3770-3782.
39. Keay J., Bridgham J.T., Thornton J.W. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 2006, 147:3861-3869.
40. Keay J., Thornton J.W. Hormone-activated estrogen receptors in annelid invertebrates: implications for evolution and endocrine disruption. Endocrinology 2009, 150:1731-1738.
41. Khersonsky O., Roodveldt C., Tawfik D.S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 2006, 10:498-508.
42. 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, 67:59-77.
43. King-Jones K., Horner M.A., Lam G., Thummel C.S. The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell. Metab. 2006, 4:37-48.
44. Krylova I.N., Sablin E.P., Moore J., Xu R.X., Waitt G.M., MacKay J.A., Juzumiene D., Bynum J.M., Madauss K., Montana V., Lebedeva L., Suzawa M., Williams J.D., Williams S.P., Guy R.K., Thornton J.W., Fletterick R.J., Willson T.M., Ingraham H.A. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell 2005, 120:343-355.
45. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Häggblad J., Nilsson S., Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138:863-870.
46. Lafont R., Mathieu M. Steroids in aquatic invertebrates. Ecotoxicology 2007, 16:109-130.
47. Laudet V., Hänni C., Coll J., Catzeflis F., Stéhelin D. Evolution of the nuclear receptor gene superfamily. EMBO J. 1992, 11:1003-1013.
48. Laudet V. Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J. Mol. Endocrinol. 1997, 19:207-226.
49. Lindblom T.H., Pierce G.J., Sluder A.E. A C. elegans orphan nuclear receptor contributes to xenobiotic resistance. Curr. Biol. 2001, 11:864-868.
50. Makishima M., Lu T.T., Xie W., Whitfield G.K., Domoto H., Evans R.M., Haussler M.R., Mangelsdorf D.J. Vitamin D receptor as an intestinal bile acid sensor. Science 2002, 296:1313-1316.
51. Markov G., Lecointre G., Demeneix B., Laudet V. The " street light syndrome", or how protein taxonomy can bias experimental manipulations. Bioessays 2008, 30:349-357.
52. Markov G.V., Paris M., Bertrand S., Laudet V. The evolution of the ligand/receptor couple: a long road from comparative endocrinology to comparative genomics. Mol. Cell. Endocrinol. 2008, 293:5-16.
53. Markov G.V., Tavares R., Dauphin-Villemant C., Demeneix B.A., Baker M.E., Laudet V. Independent elaboration of steroid hormone signaling pathways in metazoans. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11913-11918.
54. Mic F.A., Molotkov A., Benbrook D.M., Duester G. Retinoid activation of retinoic acid receptor but not retinoid X receptor is sufficient to rescue lethal defect in retinoic acid synthesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7135-7140.
55. Mizuta T., Kubokawa K. Presence of sex steroids and cytochrome P450 genes in amphioxus. Endocrinology 2007, 148:3554-3565.
56. Mizuta T., Asahina K., Suzuki M., Kubokawa K. In vitro conversion of sex steroids and expression of sex steroidogenic enzyme genes in amphioxus ovary. J. Exp. Zool. 2008, 309A:83-93.
57. Moore D.D. Diversity and unity in the nuclear hormone receptors: a terpenoid receptor superfamily. New Biol. 1990, 2:100-105.
58. Mukaiyama Y., Uchida T., Sato E., Sasaki A., Sato Y., Igarashi J., Kurokawa H., Sagami I., Kitagawa T., Shimizu T. Spectroscopic and DNA-binding characterization of the isolated heme-bound basic helix-loop-helix-PAS-A domain of neuronal PAS protein 2 (NPAS2), a transcription activator protein associated with circadian rhythms. FEBS J. 2006, 273:2528-2539.
59. Nuclear Receptors Nomenclature Committee A unified nomenclature system for the nuclear receptor superfamily. Cell 1999, 97:161-163.
60. O'Malley B.W. Did eucaryotic steroid receptors evolve from intracrine gene regulators?. Endocrinology 1989, 125:1119-1120.
61. Paris M., Escriva H., Schubert M., Brunet F., Brtko J., Cieselski F., Roecklin D., Vivat-Hannah V., Cravedi J.-P., Scanlan T.S., Renaud J.-P., Holland N.D., Laudet V. Amphioxus metamorphosis and the origin of the thyroid hormone signaling pathway. Curr. Biol. 2008, 18:825-830.
62. Paris M., Pettersson K., Schubert M., Bertrand S., Pongratz I., Escriva H., Laudet V. An amphioxus orthologue of the estrogen receptor that does not bind estradiol: insight into estrogen receptor evolution. BMC Evol. Biol. 2008, 8:219.
63. Reitzel A.M., Tarrant A.M. Nuclear receptor complement of the cnidarian Nematostella vectensis: phylogenetic relationships and developmental expression patterns. BMC Evol. Biol. 2009, 9:230.
64. Reitzel A.M., Tarrant A.M. Correlated evolution of androgen receptor and aromatase revisited. Mol. Biol. Evol. 2010, 27:2211-2215.
65. Reschly E.J., Ai N., Welsh W.J., Ekins S., Hagey L.R., Krasowski M.D. Ligand specificity and evolution of liver X receptors. J. Steroid Biochem. Mol. Biol. 2008, 110:83-94.
66. Reschly E.J., Ai N., Ekins S., Welsh W.J., Hagey L.R., Hofmann A.F., Krasowski M.D. Evolution of the bile salt nuclear receptor FXR in vertebrates. J. Lipid Res. 2008, 49:1577-1587.
67. Rochette-Egly C. Nuclear receptors: integration of multiple signalling pathways through phosphorylation. Cell Signal. 2003, 15:355-366.
68. Schubert M., Brunet F., Paris M., Bertrand S., Benoit G., Laudet V. Nuclear hormone receptor signaling in amphioxus. Dev. Genes Evol. 2008, 218:651-665.
69. Schug T.T., Berry D.C., Shaw N.S., Travis S.N., Noy N. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 2007, 129:723-733.
70. Sladek F. Desperately seeking ...something. Mol. Cell 2002, 10:219-221.
71. Sladek, F.M., What are nuclear receptor ligands? Mol. Cell. Endocrinol. doi:10.1016/j.mce.2010.06.018.
72. Stout E.P., Clair J.J.L., Snell T.W., Shearer T.L., Kubanek J. Conservation of progesterone hormone function in invertebrate reproduction. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11859-11864.
73. Theodosiou M., Laudet V., Schubert M. From carrot to clinic: an overview of the retinoic signaling pathway. Cell. Mol. Life Sci. 2010, 67:1423-1445.
74. Thomas J.H. Rapid birth-death evolution specific to xenobiotic cytochrome P450 genes in vertebrates. PLoS Genet. 2007, 3:e67.
75. Thornton J.W. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5671-5676.
76. Thornton J.W., Need E., Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 2003, 301:1714-1717.
77. Tzertzinis G., Egaña A.L., Palli S.R., Robinson-Rechavi M., Gissendanner C.R., Liu C., Unnasch T.R., Maina C.V. Molecular evidence for a functional ecdysone signaling system in Brugia malayi. PLoS Negl. Trop. Dis. 2010, 4:e625.
78. Wada T., Gao J., Xie W. PXR and CAR in energy metabolism. Trends Endocrinol. Metab. 2009, 20:273-279.
79. Weihua Z., Lathe R., Warner M., Gustafsson J.A. An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta,17beta-diol, and CYP7B1, regulates prostate growth. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13589-13594.
80. Whitfield G.K., Dang H.T.L., Schluter S.F., Bernstein R.M., Bunag T., Manzon L.A., Hsieh G., Dominguez C.E., Youson J.H., Haussler M.R., Marchalonis J.J. Cloning of a functional vitamin D receptor from the lamprey (Petromyzon marinus), an ancient vertebrate lacking a calcified skeleton and teeth. Endocrinology 2003, 144:2704-2716.
81. Yuan X., Ta T.C., Lin M., Evans J.R., Dong Y., Bolotin E., Sherman M.A., Forman B.M., Sladek F.M. Identification of an endogenous ligand bound to a native orphan nuclear receptor. PLoS One 2009, 4:e5609.
82. Zimmerman A.W., Veerkamp J.H. New insights into the structure and function of fatty acid-binding proteins. Cell. Mol. Life Sci. 2002, 59:1096-1116.