An amphioxus orthologue of the estrogen receptor that does not bind estradiol: Insights into estrogen receptor evolution

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Paris, Mathilde ^a   Pettersson, Katarina ^b   Schubert, Michael ^a   Bertrand, Stephanie ^c   Pongratz, Ingemar ^b   Escriva, Hector ^c   Laudet, Vincent ^a  

^a UNIVERSITÉ DE LYON   (France)

^b KAROLINSKA INSTITUTE   (Sweden)

^c LABORATOIRE ARAGO   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; 4,4' ISOPROPYLIDENEDIPHENOL; PHENOL DERIVATIVE;

ARTICLE; DNA BINDING; ENDOPLASMIC RETICULUM; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARSIMONY ANALYSIS; PHYLOGENY; PROTEIN DEGRADATION; REPORTER GENE; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; COMPARATIVE STUDY; DNA RESPONSIVE ELEMENT; GENETICS; HUMAN; INVERTEBRATE CHORDATA; METABOLISM; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PETROMYZON; SEQUENCE ALIGNMENT; TRANSACTIVATION;

BRANCHIOSTOMA FLORIDAE; BRANCHIOSTOMA LANCEOLATUM; PETROMYZON MARINUS; PETROMYZONTIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHORDATA, NONVERTEBRATE; CLONING, MOLECULAR; ESTRADIOL; EVOLUTION, MOLECULAR; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; PETROMYZON; PHENOLS; PHYLOGENY; RECEPTORS, ESTROGEN; RESPONSE ELEMENTS; SEQUENCE ALIGNMENT; TRANS-ACTIVATION (GENETICS);

EID: 51249118917     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-219     Document Type: Article

References (94)

1. Principles for modulation of the nuclear receptor superfamily. H Gronemeyer JA Gustafsson V Laudet, Nat Rev Drug Discov 2004 3 950 964 10.1038/nrd1551 15520817
2. The Nuclear Receptor FacsBook. V Laudet H Gronemeyer, London: Academic Press; 2005
3. Overview of nomenclature of nuclear receptors. P Germain B Staels C Dacquet M Spedding V Laudet, Pharmacological reviews 2006 58 685 704 10.1124/pr.58.4.2 17132848
4. International Union of Pharmacology. LXVI. Orphan nuclear receptors. G Benoit A Cooney V Giguere H Ingraham M Lazar G Muscat T Perlmann JP Renaud J Schwabe F Sladek MJ Tsai V Laudet, Pharmacological reviews 2006 58 798 836 10.1124/pr.58.4.10 17132856
5. Crystal structure of the HNF4 alpha ligand binding domain in complex with endogenous fatty acid ligand. S Dhe-Paganon K Duda M Iwamoto YI Chi SE Shoelson, The Journal of biological chemistry 2002 277 37973 37976 10.1074/jbc.C200420200 12193589
6. Hepatocyte nuclear factor 4 is a transcription factor that constitutively binds fatty acids. GB Wisely AB Miller RG Davis AD Thornquest Jr R Johnson T Spitzer A Sefler B Shearer JT Moore AB Miller TM Willson SP Williams, Structure 2002 10 1225 1234 10.1016/S0969-2126(02)00829-8 12220494
7. Ligand binding and nuclear receptor evolution. H Escriva F Delaunay V Laudet, Bioessays 2000 22 717 727 10.1002/1521-1878(200008)22:8<717::AID- BIES5>3.0.CO;2-I 10918302
8. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. JW Thornton, Proceedings of the National Academy of Sciences of the United States of America 2001 98 5671 5676 11331759 10.1073/pnas.091553298
9. The evolution of the nuclear receptor superfamily. H Escriva S Bertrand V Laudet, Essays in biochemistry 2004 40 11 26 15242336
10. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. IN Krylova EP Sablin J Moore RX Xu GM Waitt JA MacKay D Juzumiene JM Bynum K Madauss V Montana L Lebedeva M Suzawa JD Williams SP Williams RK Guy JW Thornton RJ Fletterick TM Willson HA Ingraham, Cell 2005 120 343 355 10.1016/j.cell.2005.01.024 15707893
11. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. JW Thornton E Need D Crews, Science 2003 301 5640 1714 1717 14500980 10.1126/science.1086185
12. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. J Keay JT Bridgham JW Thornton, Endocrinology 2006 147 3861 3869 10.1210/en.2006-0363 16690796
13. Neofunctionalization in vertebrates: the example of retinoic acid receptors. H Escriva S Bertrand P Germain M Robinson-Rechavi M Umbhauer J Cartry M Duffraisse L Holland H Gronemeyer V Laudet, PLoS genetics 2006 2 e102 16839186 10.1371/journal.pgen.0020102
14. Evolution of adrenal and sex steroid action in vertebrates: a ligand-based mechanism for complexity. ME Baker, Bioessays 2003 25 396 400 10.1002/bies.10252 12655646
15. Presence of sex steroids and cytochrome P450 (CYP) genes in amphioxus. T Mizuta K Kubokawa, Endocrinology 2007 17446181
16. Crystal structure of an ancient protein: evolution by conformational epistasis. EA Ortlund JT Bridgham MR Redinbo JW Thornton, Science 2007 317 5844 1544 1548 17702911 10.1126/science.1142819
17. An evolvable oestrogen receptor activity sensor: development of a modular system for integrating multiple genes into the yeast genome. JE Fox JT Bridgham TF Bovee JW Thornton, Yeast (Chichester, England) 2007 24 379 390 10.1002/yea.1466 17345582
18. Ligand binding was acquired during evolution of nuclear receptors. H Escriva R Safi C Hanni MC Langlois P Saumitou-Laprade D Stehelin A Capron R Pierce V Laudet, Proceedings of the National Academy of Sciences of the United States of America 1997 94 6803 6808 9192646 10.1073/pnas.94.13.6803
19. Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. V Laudet, Journal of molecular endocrinology 1997 19 207 226 10.1677/jme.0.0190207 9460643
20. Analysis of 3D models of octopus estrogen receptor with estradiol: evidence for steric clashes that prevent estrogen binding. ME Baker C Chandsawangbhuwana, Biochem Biophys Res Commun 2007 361 782 788 17678875 10.1016/j.bbrc.2007.07.110
21. Amphioxus, a primitive chordate, is on steroids: evidence for sex steroids and steroidogenic enzymes. ME Baker, Endocrinology 2007 148 3551 3553 10.1210/en.2007-0547 17639030
22. Recent insights into the origins of adrenal and sex steroid receptors. ME Baker, Journal of molecular endocrinology 2002 28 149 152 10.1677/jme.0.0280149 12063181
23. A unified nomenclature system for the nuclear receptor superfamily. NRN committee, Cell 1999 97 161 163 10.1016/S0092-8674(00)80726-6 10219237
24. Tissue preferential expression of estrogen receptor gene in the marine snail, Thais clavigera. M Kajiwara S Kuraku T Kurokawa K Kato S Toda H Hirose S Takahashi Y Shibata T Iguchi T Matsumoto T Miyata T Miura Y Takahashi, Gen Comp Endocrinol 2006 148 315 326 16782100 10.1016/j.ygcen.2006.03.016
25. Oyster estrogen receptor: cDNA cloning and immunolocalization. T Matsumoto AM Nakamura K Mori I Akiyama H Hirose Y Takahashi, Gen Comp Endocrinol 2007 151 195 201 17324427 10.1016/j.ygcen.2007.01.016
26. Novel estrogen receptor-related Transcripts in Marisa cornuarietis; a freshwater snail with reported sensitivity to estrogenic chemicals. R Bannister N Beresford D May EJ Routledge S Jobling M Rand-Weaver, Environmental science & technology 2007 41 2643 2650 10.1021/es062565m 17438828
27. Tunicates and not cephalochordates are the closest living relatives of vertebrates. F Delsuc H Brinkmann D Chourrout H Philippe, Nature 2006 439 965 968 10.1038/nature04336 16495997
28. Retinoic acid signaling and the evolution of chordates. F Marletaz LZ Holland V Laudet M Schubert, International journal of biological sciences 2006 2 38 47 16733532
29. Molecular phylogeny and divergence times of deuterostome animals. JE Blair SB Hedges, Mol Biol Evol 2005 22 2275 2284 16049193 10.1093/molbev/msi225
30. Amphioxus and tunicates as evolutionary model systems. M Schubert H Escriva J Xavier-Neto V Laudet, Trends in ecology & evolution (Personal edition) 2006 21 269 277 16697913
31. The Ciona intestinalis genome: when the constraints are off. LZ Holland JJ Gibson-Brown, Bioessays 2003 25 529 532 10.1002/bies.10302 12766941
32. Organization of Hox genes in ascidians: present, past, and future. T Ikuta H Saiga, Dev Dyn 2005 233 382 389 10.1002/dvdy.20374 15844201
33. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. P Dehal Y Satou RK Campbell J Chapman B Degnan A De Tomaso B Davidson A Di Gregorio M Gelpke DM Goodstein N Harafuji KE Hastings I Ho K Hotta W Huang T Kawashima P Lemaire D Martinez IA Meinertzhagen S Necula M Nonaka N Putnam S Rash H Saiga M Satake A Terry L Yamada HG Wang S Awazu K Azumi, Science 2002 298 2157 2167 12481130 10.1126/science.1080049
34. Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus. M Howard-Ashby SC Materna CT Brown L Chen RA Cameron EH Davidson, Developmental biology 2006 300 90 107 10.1016/j.ydbio.2006.08.033 17054934
35. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. LZ Holland R Albalat K Azumi E Benito-Gutiérrez MJ Blow M Bronner-Fraser F Brunet T Butts S Candiani LJ Dishaw DE Ferrier J Garcia-Fernàndez JJ Gibson-Brown C Gissi A Godzik F Hallböök D Hirose K Hosomichi T Ikuta H Inoko M Kasahara J Kasamatsu T Kawashima A Kimura M Kobayashi Z Kozmik K Kubokawa V Laudet GW Litman AC Mchardy D Meulemans M Nonaka RP Olinski Z Pancer LA Pennacchio JP Rast I Rigoutsos M Robinson-Rechavi G Roch H Saiga Y Sasakura M Satake Y Satou M Schubert N Sherwood T Shiina N Takatori J Tello P Vopalensky S Wada A Xu Y Ye K Yoshida F Yoshizaki JK Yu Q Zhang CM Zmasek PJ de Jong K Osoegawa NH Putnam DS Rokhsar N Satoh PW Holland, Genome Res 2008 18 1100 1111 18562680 10.1101/gr.073676.107
36. Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition. PL Bardet M Schubert B Horard LZ Holland V Laudet ND Holland JM Vanacker, Evolution & development 2005 7 223 233 10.1111/j.1525-142X.2005.05025.x 15876195
37. Cases in which parsimony or compatibility methods will be positively misleading. J Felsenstein, Systematic zoology 1978 27 401 410 10.2307/2412923
38. CONSEL: for assessing the confidence of phylogenetic tree selection. H Shimodaira M Hasegawa, Bioinformatics (Oxford, England) 2001 17 1246 1247 10.1093/bioinformatics/17.12.1246 11751242
39. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. M Anisimova O Gascuel, Systematic biology 2006 55 539 552 10.1080/10635150600755453 16785212
40. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Systematic biology 2003 52 696 704 10.1080/10635150390235520 14530136
41. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. N Lartillot H Brinkmann H Philippe, BMC evolutionary biology 2007 7 Suppl 1 S4 17288577 10.1186/1471-2148-7-S1-S4
42. Genomic analysis of the nuclear receptor family: new insights into structure, regulation, and evolution from the rat genome. Z Zhang PE Burch AJ Cooney RB Lanz FA Pereira J Wu RA Gibbs G Weinstock DA Wheeler, Genome research 2004 14 580 590 15059999 10.1101/gr.2160004
43. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. GG Kuiper B Carlsson K Grandien E Enmark J Haggblad S Nilsson JA Gustafsson, Endocrinology 1997 138 863 870 10.1210/en.138.3.863 9048584
44. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. BD Gehm JM McAndrews PY Chien JL Jameson, Proceedings of the National Academy of Sciences of the United States of America 1997 94 14138 14143 9391166 10.1073/pnas.94.25.14138
45. Mammalian phytoestrogens: enterodiol and enterolactone. LQ Wang, Journal of chromatography 2002 777 289 309 10.1016/S1570-0232(02)00281-7 12270221
46. International Union of Pharmacology. LXIV. Estrogen receptors. K Dahlman-Wright V Cavailles SA Fuqua VC Jordan JA Katzenellenbogen KS Korach A Maggi M Muramatsu MG Parker JA Gustafsson, Pharmacological reviews 2006 58 773 781 10.1124/pr.58.4.8 17132854
47. In vitro molecular mechanisms of bisphenol A action. YB Wetherill BT Akingbemi J Kanno JA McLachlan A Nadal C Sonnenschein CS Watson RT Zoeller SM Belcher, Reprod Toxicol 2007 24 178 198 17628395 10.1016/j.reprotox.2007.05.010
48. PAML 4: phylogenetic analysis by maximum likelihood. Z Yang, Mol Biol Evol 2007 24 1586 1591 17483113 10.1093/molbev/msm088
49. Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. DM Tanenbaum Y Wang SP Williams PB Sigler, Proceedings of the National Academy of Sciences of the United States of America 1998 95 5998 6003 9600906 10.1073/pnas.95.11.5998
50. Identification of amino acids in the hormone binding domain of the human estrogen receptor important in estrogen binding. K Ekena KE Weis JA Katzenellenbogen BS Katzenellenbogen, The Journal of biological chemistry 1996 271 20053 20059 10.1074/jbc.271.33.20053 8702724
51. Differential interactions of estrogens and antiestrogens at the 17 beta-hydroxyl or counterpart hydroxyl with histidine 524 of the human estrogen receptor alpha. S Aliau H Mattras E Richard JC Bonnafous JL Borgna, Biochemistry 2002 41 7979 7988 10.1021/bi0121914 12069588
52. Motif analysis of amphioxus, lamprey and invertebrate estrogen receptors: toward a better understanding of estrogen receptor evolution. ME Baker C Chandsawangbhuwana, Biochem Biophys Res Commun 2008 371 724 728 18471435 10.1016/j.bbrc.2008.04.152
53. Molecular basis of agonism and antagonism in the oestrogen receptor. AM Brzozowski AC Pike Z Dauter RE Hubbard T Bonn O Engstrom L Ohman GL Greene JA Gustafsson M Carlquist, Nature 1997 389 753 758 10.1038/39645 9338790
54. Distribution plasticity of the human estrogen receptor alpha in live cells: distinct imaging of consecutively expressed receptors. H Pick H Jankevics H Vogel, Journal of molecular biology 2007 374 1213 1223 10.1016/j.jmb.2007.10. 007 17991486
55. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. AK Shiau D Barstad PM Loria L Cheng PJ Kushner DA Agard GL Greene, Cell 1998 95 927 937 10.1016/S0092-8674(00) 81717-1 9875847
56. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. RT Nolte GB Wisely S Westin JE Cobb MH Lambert R Kurokawa MG Rosenfeld TM Willson CK Glass MV Milburn, Nature 1998 395 137 143 10.1038/25931 9744270
57. Evolution by gene duplication. S Ohno, Berlin, New York,: Springer-Verlag; 1970
58. Steroid receptor interactions with heat shock protein and immunophilin chaperones. WB Pratt DO Toft, Endocrine reviews 1997 18 306 360 10.1210/er.18.3.306 9183567
59. Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. H Greschik JM Wurtz S Sanglier W Bourguet A van Dorsselaer D Moras JP Renaud, Molecular cell 2002 9 303 313 10.1016/S1097-2765(02)00444-6 11864604
60. In vitro conversion of androgen to estrogen in amphioxus gonadal tissues. GV Callard JA Pudney SL Kendall R Reinboth, Gen Comp Endocrinol 1984 56 53 58 6541606 10.1016/0016-6480(84)90060-1
61. The genomic environment around the Aromatase gene: evolutionary insights. LF Castro MM Santos MA Reis-Henriques, BMC evolutionary biology 2005 5 43 16098224 10.1186/1471-2148-5-43
62. Co-evolution of steroidogenic and steroid-inactivating enzymes and adrenal and sex steroid receptors. ME Baker, Mol Cell Endocrinol 2004 215 55 62 15026175 10.1016/j.mce.2003.11.007
63. Comparison of synthesis of 15 alpha-hydroxylated steroids in males of four North American lamprey species. MB Bryan BA Young DA Close J Semeyn TC Robinson J Bayer W Li, Gen Comp Endocrinol 2006 146 149 156 16359676 10.1016/j.ygcen.2005.11.003
64. Amphioxus Postembryonic Development Reveals the Homology of Chordate Metamorphosis. M Paris H Escriva M Schubert F Brunet J Brtko F Ciesielski D Roecklin V Vivat-Hannah EL Jamin J-P Cravedi TS Scanlan J-P Renaud ND Holland V Laudet, Current Biology 2008 18 825 830 10.1016/j.cub.2008.04.078 18514519
65. Nongenomic actions of steroid hormones. R Losel M Wehling, Nature reviews 2003 4 46 56 10.1038/nrm1009 12511868
66. Non-genomic steroid hormone effects: membrane or intracellular receptors? M Wehling R Losel, J Steroid Biochem Mol Biol 2006 102 180 183 17113980 10.1016/j.jsbmb.2006.09.016
67. Nongenomic steroid action: controversies, questions, and answers. RM Losel E Falkenstein M Feuring A Schultz HC Tillmann K Rossol-Haseroth M Wehling, Physiological reviews 2003 83 965 1016 12843413
68. The sea lamprey (Petromyzon marinus) has a receptor for androstenedione. MB Bryan AP Scott W Li, Biology of reproduction 2007 77 688 696 10.1095/biolreprod.107.061093 17596561
69. Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor alpha subtypes and their evolutionary origins. P Thomas Y Pang J Dong P Groenen J Kelder J de Vlieg Y Zhu C Tubbs, Endocrinology 2007 148 705 718 10.1210/en.2006-0974 17082257
70. Resurrecting ancient genes: experimental analysis of extinct molecules. JW Thornton, Nat Rev Genet 2004 5 366 375 10.1038/nrg1324 15143319
71. Evolution of hormone-receptor complexity by molecular exploitation. JT Bridgham SM Carroll JW Thornton, Science 2006 312 5770 97 101 16601189 10.1126/science.1123348
72. Assessing the accuracy of ancestral protein reconstruction methods. PD Williams DD Pollock BP Blackburne RA Goldstein, PLoS computational biology 2006 2 e69 16789817 10.1371/journal.pcbi.0020069
73. Characterization of the Nurr1 ligand-binding domain co-activator interaction surface. N Volakakis M Malewicz B Kadkhodai T Perlmann G Benoit, Journal of molecular endocrinology 2006 37 317 326 10.1677/jme.1.02106 17032747
74. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. T Iwema IM Billas Y Beck F Bonneton H Nierengarten A Chaumot G Richards V Laudet D Moras, The EMBO journal 2007 26 3770 3782 10.1038/sj.emboj.7601810 17673910
75. Steroids in aquatic invertebrates. R Lafont M Mathieu, Ecotoxicology (London, England) 2007 16 109 130 17238002
76. Evolution of oestrogen functions in vertebrates. IG Lange A Hartel HH Meyer, J Steroid Biochem Mol Biol 2002 83 219 226 12650719 10.1016/S0960- 0760(02)00225-X
77. International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. NZ Lu SE Wardell KL Burnstein D Defranco PJ Fuller V Giguere RB Hochberg L McKay JM Renoir NL Weigel EM Wilson DP McDonnell JA Cidlowski, Pharmacological reviews 2006 58 782 797 10.1124/pr.58.4.9 17132855
78. Molecular cloning and characterization of a nuclear androgen receptor activated by 11-ketotestosterone. PE Olsson AH Berg J von Hofsten B Grahn A Hellqvist A Larsson J Karlsson C Modig B Borg P Thomas, Reprod Biol Endocrinol 2005 3 37 16107211 10.1186/1477-7827-3-37
79. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. O Jaillon JM Aury F Brunet JL Petit N Stange-Thomann E Mauceli L Bouneau C Fischer C Ozouf-Costaz A Bernot S Nicaud D Jaffe S Fisher G Lutfalla C Dossat B Segurens C Dasilva M Salanoubat M Levy N Boudet S Castellano V Anthouard C Jubin V Castelli M Katinka B Vacherie C Biemont Z Skalli L Cattolico J Poulain, Nature 2004 431 946 957 10.1038/nature03025 15496914
80. Sex steroids and their receptors in lampreys. MB Bryan AP Scott W Li, Steroids 2008 73 1 12 10.1016/j.steroids.2007.08.011 17931674
81. The evolution of the ligand/receptor couple: A long road from comparative endocrinology to comparative genomics. G Markov M Paris S Bertrand V Laudet, Molecular and Cellular Endocrinology 2008 18634845 10.1016/j.mce.2008.06.011
82. The «street light syndrome», or how protein taxonomy can bias experimental manipulations. G Markov G Lecointre B Demeneix V Laudet, Bioessays 2008 30 349 357 10.1002/bies.20730 18348179
83. Evolution of the bile salt nuclear receptor FXR in vertebrates. EJ Reschly N Ai S Ekins WJ Welsh LR Hagey AF Hofmann MD Krasowski, Journal of lipid research 2008 18362391
84. Ligand specificity and evolution of liver × receptors. EJ Reschly N Ai WJ Welsh S Ekins LR Hagey MD Krasowski, J Steroid Biochem Mol Biol 2008 18395439
85. Functional evolution of the vitamin D and pregnane × receptors. EJ Reschly AC Bainy JJ Mattos LR Hagey N Bahary SR Mada J Ou R Venkataramanan MD Krasowski, BMC evolutionary biology 2007 7 222 17997857 10.1186/1471-2148-7-222
86. Functional evolution of the pregnane × receptor. M Iyer EJ Reschly MD Krasowski, Expert opinion on drug metabolism & toxicology 2006 2 381 397 16863441 10.1517/17425255.2.3.381
87. Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. F Delaunay K Pettersson M Tujague JA Gustafsson, Molecular pharmacology 2000 58 584 590 10953052
88. Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. P Penttinen J Jaehrling AE Damdimopoulos J Inzunza JG Lemmen P van der Saag K Pettersson G Gauglitz S Makela I Pongratz, Endocrinology 2007 148 4875 4886 10.1210/en.2007-0289 17628008
89. MUSCLE: multiple sequence alignment with high accuracy and high throughput. RC Edgar, Nucleic acids research 2004 32 1792 1797 15034147 10.1093/nar/gkh340
90. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. N Galtier M Gouy C Gautier, Comput Appl Biosci 1996 12 543 548 9021275
91. Confidence limits on phylogenies: An approach using the bootstrap. J Felsenstein, Evolution 1985 39 783 791 10.2307/2408678
92. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. DL Swofford PJ Waddell JP Huelsenbeck PG Foster PO Lewis JS Rogers, Systematic biology 2001 50 525 539 10.1080/106351501750435086 12116651
93. Conserved RARE localization in amphioxus Hox clusters and implications for Hox code evolution in the vertebrate neural crest. H Wada H Escriva S Zhang V Laudet, Dev Dyn 2006 235 1522 1531 10.1002/dvdy.20730 16538655
94. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Z Wang G Benoit J Liu S Prasad P Aarnisalo X Liu H Xu NP Walker T Perlmann, Nature 2003 423 555 560 10.1038/nature01645 12774125