Nuclear receptor complement of the cnidarian Nematostella vectensis: Phylogenetic relationships and developmental expression patterns

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Reitzel, Adam M ^a   Tarrant, Ann M ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; DNA; CELL RECEPTOR;

ARTICLE; DNA BINDING; GENOMICS; LIGAND BINDING; METAZOON; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEA ANEMONE; ANIMAL; GENETICS;

ANIMALIA; BILATERIA; CNIDARIA; DEUTEROSTOMIA; METAZOA; NEMATOSTELLA VECTENSIS; PROTOSTOMIA;

ANIMALS; PHYLOGENY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEA ANEMONES;

EID: 70349577811     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-230     Document Type: Article

References (92)

1. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. C Larroux B Fahey D Liubicich V Hinman M Gauthier M Gongora K Green G Wörheide S Leys B Degnan, Evolution and Development 2006 8 150 173 10.1111/j.1525-142X.2006.00086.x 16509894
2. Retinoid × receptor and retinoic acid response in the marine sponge Suberites domuncula. M Wiens R Batel M Korzhev W Müller, Journal of Experimental Biology 2003 206 3261 71 10.1242/jeb.00541 12909707
3. The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. D Gauchat H Escriva M Miljkovic-Licina S Chera M-C Langlois A Begue V Laudet B Galliot, Developmental Biology 2004 275 104 23 10.1016/j.ydbio.2004.07.037 15464576
4. The evolution of nuclear receptors: evidence from the coral Acropora. L Grasso D Hayward J Trueman K Hardie P Janssens E Ball, Molecular Phylogenetics and Evolution 2001 21 93 102 10.1006/mpev.2001.0994 11603940
5. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. S Bertrand F Brunet H Escriva G Parmentier V Laudet M Robinson-Rechavi, Molecular Biology and Evolution 2004 21 1923 37 10.1093/molbev/msh200 15229292
6. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. N King MJ Westbrook SL Young A Kuo M Abedin J Chapman S Fairclough U Hellsten Y Isogai I Letunic, et al. Nature 2008 451 783 788 10.1038/nature06617 18273011
7. The nuclear receptor superfamily has undergone extensive proliferation and diversification in nematodes. A Sluder S Matthews D Hough V Yin C Maina, Genome Research 1999 9 103 20 10022975
8. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. J Keay J Bridgham J Thornton, Endocrinology 2006 147 3861 9 10.1210/en.2006-0363 16690796
9. Schistosoma mansoni (Platyhelminthes, Trematoda) nuclear receptors: Sixteen new members and a novel subfamily. W Wu EG Niles N El-Sayed M Berriman PT LoVerde, Gene 2006 366 303 315 10.1016/j.gene.2005.09.013 16406405
10. Evolution of a novel subfamily of nuclear receptors with members that each contain two DNA binding domains. W Wu EG Niles H Hirai PT LoVerde, BMC Evolutionary Biology 2007 7 27 10.1186/1471-2148-7-27 17319953
11. Retinoic acid × receptor in the diploblast, Tripedalia cystophora. Z Kostrouch M Kostrouchova W Love E Jannini J Piatigorsky J Rall, Proceedings of the National Academy of Science, USA 1998 95 13442 7 10.1073/pnas.95.23.13442 (Pubitemid 28522991)
12. Estrone and estradiol-17 concentration in tissue of the scleractinian coral, Montipora verrucosa. A Tarrant S Atkinson M Atkinson, Comparative Biochemistry and Physiology A 1999 122
13. Sex steroids in scleractinian coral, Euphyllia ancora: implication in mass spawning. W-H Twan J-S Hwang C-F Chang, Biol Reprod 2003 68 2255 60 10.1095/biolreprod.102.012450 12606339
14. Chemical signals in gametogenesis, spawning, and larval settlement and defense of the soft coral Sinularia polydactyla. M Slattery G Hines J Starmer V Paul, Coral Reefs 1999 18 75 84 10.1007/s003380050158 (Pubitemid 29358026)
15. Annual variations and sex-related differences of estradiol-17beta levels in the anthozoan Renilla koellikeri. V Pernet M Anctil, General and Comparative Endocrinology 2002 129 63 8 10.1016/S0016-6480(02)00513-0 12409097
16. Diterpenoids from Caribbean gorgonians act as noncompetitive inhibitors of the nicotinic acetylcholine receptor. V Eterovic R Hann P Ferchmin A Rodriques L Li Y Lee M McNamee, Cell Mol Neurobiol 1993 13 99 110 10.1007/BF00735367 8102324
17. New hemiketal steroid from the introduced soft coral Chromonephthea braziliensis is a chemical defense against predatory fishes. B Fleury B Lages J Barbosa C Kaiser A Pinto, Journal of Chemical Ecology 2008 34 987 93 10.1007/s10886-008-9499-y 18584259
18. The basis of prostaglandin synthesis in coral. R Koljak I Järving R Kurg W Boeglin K Varvas K Valmsen M Ustav A Brash N Samel, Journal of Biological Chemistry 2001 276 7033 40 10.1074/jbc.M009803200 11085996
19. Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. AA Sullivan CS Thummel, Mol Endocrinol 2003 17 2125 2137 10.1210/me.2002-0430 12881508
20. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. N Putnam M Srivastava U Hellsten B Dirks J Chapman A Salamov A Terry H Shapiro E Lindquist V Kapitonov, et al. Science 2007 317 86 94 10.1126/science.1139158 17615350
21. Nuclear receptor diversity: phylogeny, evolution and endocrine disruption. JW Thornton, Pure and Applied Chemistry 2003 75 1827 1839 10.1351/pac200375111827
22. Comparison of the complete nuclear receptor sets from the human, Caenorhabditis elegans, and Drosophila genomes. J Maglich A Sluder X Guan Y Shi D McKee K Carrick K Kamdar T Willson J Moore, Genome Biology 2001 2 1 7 10.1186/gb-2001-2-8-research0029
23. Liver-enriched transcription factors HNF-4 is a novel member of the steroid hormone receptor superfamily. F Sladek W Zhong E Lai J Darnell, Genes Dev 1990 4 2353 65 10.1101/gad.4.12b.2353 2279702
24. Crystal structure of the HNF4 alpha ligand binding domain in complex with endogenous fatty acid ligand. S Dhe-Paganon K Duda M Iwamoto Y Chi S Shoelson, Journal of Biological Chemistry 2002 277 37973 6 10.1074/jbc.C200420200 12193589
25. Hepatocyte nuclear factor 4 is a transcription factor that constitutively binds fatty acids. G Wisely A Miller R Davis AJ Thornquest R Johnson T Spitzer A Sefler B Shearer J Moore A Miller, et al. Structure 2002 10 1225 34 10.1016/S0969-2126(02)00829-8 12220494
26. HNF4: a central regulator of hepatocyte differentiation and function. A Watt W Garrison S Duncan, Hepatology 2003 37 1249 53 10.1053/jhep.2003.50273 12774000
27. The expression patttern of a Drosophila homolog to the mouse transcription factor HNF-4 suggests a determinative role in gut formation. W Zhong F Sladek J Darnell, The EMBO Journal 1993 12 537 44 8440243
28. Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. M Robinson-Rechavi C Maina C Gissendanne V Laudet A Sluder, Journal of Molecular Evolution 2004 60 577 86 10.1007/s00239-004-0175-8
29. Nuclear hormone receptor NHR-49 controls fat consumption, storage, and composition in C. elegans. MR Van Gilst H Hadjivassiliou A Jolly KR Yamamoto, PLoS Biol 2004 3 53 10.1371/journal.pbio.0030053
30. Three orphan nuclear receptors in the scleractinian coral Pocillopora damicornis. A Tarrant J Cortés M Atkinson S Atkinson K Johanning T-C Chiang J Vargas J McLachlan, Revista de Biologia Tropical 56 Suppl 4 39 48
31. Tlx and Pax6 co-operate genetically to establish the pallio-subpallial boundary in the embryonic mouse telencephalon. J Stenman R Yu R Evans K Campbell, Development 2003 130 1113 22 10.1242/dev.00328 12571103
32. The orphan nuclear receptors Tlx regulates Pax2 and is essential for vision. R Yu M-Y Chiang T Tanabe M Kobayashi K Yasuda R Evans K Umesono, Proceedings of the National Academy of Science, USA 2000 97 2621 5 10.1073/pnas.050566897 (Pubitemid 30159220)
33. Identification of a photoreceptor cell-specific nuclear receptor. M Kobayashi S Takezawa K Hara R Yu K Umesono K Agata M Taniwaki K Yasuda K Umesono, Proceedings of the National Academy of Science, USA 1999 96 4814 9 10.1073/pnas.96.9.4814 (Pubitemid 29214494)
34. Loss of the tailless gene affects forebrain development and emotional behavior. K Roy E Thiels A Monaghan, Physiol Behav 2002 77 595 600 10.1016/S0031-9384(02)00902-2 12527005
35. Dual role of the Drosophila pattern gene tailless in embryonic termini. E Steingrimsson F Pignoni G Liaw J Lengyel, Science 1991 254 418 21 10.1126/science.1925599 1925599
36. The fax-1 nuclear hormone receptor regulates axon pathfinding and neurotransmitter expression. JW Much DJ Slade K Klampert G Garriga B Wightman, Development 2000 127 703 712 10648229
37. The C. elegans nuclear receptor gene fax-1 and homeobox gene unc-42 coordinate interneuron identity by regulating the expression of glutamate receptor subunits and other neuron-specific genes. B Wightman B Ebert N Carmean K Weber S Clever, Developmental Biology 2005 287 74 85 10.1016/j.ydbio.2005.08. 032 16183052
38. Expression and functional analysis of Nr2e3, a photoreceptor-specific nuclear receptor, suggest common mechanisms in retinal development between avians and mammals. M Kobayashi K Hara RT Yu K Yasuda, Development Genes and Evolution 2008 218 10.1007/s00427-008-0232-1 18592265
39. FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. D Matus G Thomsen M Martindale, Development Genes and Evolution 2007 217 137 148 10.1007/s00427-006-0122-3 17237944
40. Ligand binding was acquired during the evolution of nuclear receptors. H Escriva R Safi C Hanni M-C Langlois P Saumitou-Laprade D Stehelin A Capron R Pierce V Laudet, Proceedings of the National Academy of Science, USA 1997 94 6803 8 10.1073/pnas.94.13.6803 (Pubitemid 27281945)
41. Amphicoup-TF, a nuclear orphan receptor of the lancelet Branchiostoma floridae, is implicated in retinoic acid signalling pathways. M-C Langlois J-M Vanacker N Holland H Escriva C Queva V Laudet L Holland, Development, Genes and Evolution 2000 210 471 82 10.1007/s004270000087
42. SpCOUP-TF: a sea urchin member of the steroid/thyroid hormone receptor family. S-M Chan N Xu C Niemeyer J Bone C Flytzanis, Proceedings of the National Academy of Science, USA 1992 89 10568 72 10.1073/pnas.89.22.10568
43. Chicken ovalbumin upstream promoter-transcription factor (COUP-TF) modulates expression of the Purkinje cell protein-2 gene. A potential role for COUP-TF in repressing premature thyroid hormone action in the developing brain. GW Anderson RJ Larson DR Oas CR Sandhofer HL Schwartz CN Mariash JH Oppenheimer, J Biol Chem 1998 273 16391 16399 10.1074/jbc.273.26.16391 9632703
44. Sagittal band expression of COUP-TF2 gene in the developing cerebellum. M Yamamoto M Fujinuma M Tanaka UC Dräger P McCaffery, Mechanisms of Development 1999 84 143 146 10.1016/S0925-4773(99)00054-4 10473129
45. Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. B Kerber S Fellert M Hoch, Genes Dev 1998 12 1781 1786 10.1101/gad.12.12.1781 9637680
46. Functional conservation of vertebrate seven-up related genes in neurogenesis and eye development. A Fjose S Nornes U Weber M Mlodzik, The EMBO Journal 1993 12 1403 14 8467797
47. COUP-TF acts as a competitive repressor for estrogen receptor-mediated activation of the mouse lactoferrin gene. Y Liu N Yang CT Teng, Mol Cell Biol 1993 13 1836 1846 8441416
48. Cyclicity of mosquito vitellogenic ecdysteroid-mediated signaling is modulated by alternative dimerization of the RXR homolog Ultraspiraclei. J Zhu K Miuma L Chen A Raikhel, Proceedings of the National Academy of Science, USA 2003 100 544 9 10.1073/pnas.0235695100 (Pubitemid 36126088)
49. A COUP-TF/Svp homolog is highly expressed during vitellogenesis in the mosquito Aedes aegypti. K Miura J Zhu N Dittmer L Chen A Raikhel, Journal of Molecular Endocrinology 2002 29 223 38 10.1677/jme.0.0290223 12370123
50. Role of estrogen receptor ligand and estrogen response element sequence on interaction with chicken ovalbumin upstream promoter transcription factor (COUP-TF). CM Klinge, The Journal of Steroid Biochemistry and Molecular Biology 1999 71 1 19 10.1016/S0960-0760(99)00124-7 10619353
51. Evolution and developmental expression of nuclear receptor genes in the ascidian Herdmania. C Devine VF Hinman BM Degnan, International Journal of Developmental Biology 2002 46 687 692 12141458
52. Recent advances in the TR2 and TR4 orphan receptors of the nuclear receptor superfamily. Y-F Lee H-J Lee C Chang, The Journal of Steroid Biochemistry and Molecular Biology 2002 81 291 308 10.1016/S0960-0760(02)00118-8 12361719
53. Suppression of estrogen receptor-mediated transcription and cell growth by interaction with TR2 orphan receptor. Y Hu C Shyr W Che X Mu E Kim C Chang, Journal of Biological Chemistry 2002 277 33571 9 10.1074/jbc.M203531200 12093804
54. A genome-wide survey of developmental genes in Ciona intestinalis III. Genes for Fox, ETS, nuclear receptors and NF-kB. K Yagi Y Satou F Mazet S Shimeld B Degnan D Rokhsar M Levine Y Kohara N Satoh, Development, Genes and Evolution 2003 213 235 44 10.1007/s00427-003-0322-z (Pubitemid 36833692)
55. The TR2 and TR4 orphan nuclear receptors repress Gata1 transcription. O Tanabe Y Shen Q Liu AD Campbell T Kuroha M Yamamoto JD Engel, Genes Dev 2007 21 2832 2844 10.1101/gad.1593307 17974920
56. Gene Silencing by Nuclear Orphan Receptors. Y Zhang ML Dufau L Gerald, Vitamins & Hormones Academic Press 2004 68 1 48
57. Recent advances in the TR2 and TR4 orphan receptors of the nuclear receptor superfamily. Y-F Lee H-J Lee C Chang, Journal of Steroid Biochemistry and Molecular Biology 2002 81 291 308 10.1016/S0960-0760(02)00118-8 12361719
58. SmTR2/4, a Schistosoma mansoni homologue of TR2/TR4 orphan nuclear receptor. R Hu W Wu EG Niles PT LoVerde, International Journal for Parasitology 2006 36 1113 1122 10.1016/j.ijpara.2006.06.003 16839558
59. Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. A Sullivan C Thummel, Molecular Endocrinology 2003 17 2125 37 10.1210/me.2002-0430 12881508
60. The ecdysone-induced DHR4 orphan nuclear receptor coordinates growth and maturation in Drosophila. K King-Jones J-P Charles G Lam C Thummel, Cell 2005 121 773 84 10.1016/j.cell.2005.03.030 15935763
61. ATP-binding cassette protein E is involved in gene transcription and translation in Caenorhabditis elegans. Z Zhao L Fang R Johnsen D Baillie, Biochemical and Biophysical Research Communications 2004 323 104 111 10.1016/j.bbrc.2004.08.068 15351708
62. Expression of the orphan nuclear receptor, germ cell nuclear factor in mouse gonads and preimplantation embryos. Z-J Lan P Gu X Xu A Cooney, Biology of Reproduction 2003 68 282 9 10.1095/biolreprod.102.008151 12493724
63. Loss of orphan receptor Germ Cell Nuclear Factor function results in ectopic development of the tail bud and a novel posterior truncation. ACK Chung D Katz FA Pereira KJ Jackson FJ DeMayo AJ Cooney BW O'Malley, Mol Cell Biol 2001 21 663 677 10.1128/MCB.21.2.663-677.2001 11134352
64. Dimeric binding of the mouse germ cell nuclear factor. U Borgmeyer, European Journal of Biochemistry 1997 244 120 7 10.1111/j.1432-1033.1997.00120.x 9063454
65. Germ cell nuclear factor is a response element-specfic repressor of transcription. A Cooney G Hummelke T Herman F Chen K Jackson, Biochemical and Biophysical Research Communications 1998 245 94 100 10.1006/bbrc.1998.8391 9535790
66. 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
67. Hormone-Activated Estrogen Receptors in Annelid Invertebrates: Implications for Evolution and Endocrine Disruption. J Keay JW Thornton, Endocrinology 2009 150 1731 1738 10.1210/en.2008-1338 19036877
68. Trichoplax, the simplest known animal, contains an estrogen-related receptor but no estrogen receptor: Implications for estrogen receptor evolution. ME Baker, Biochemical and Biophysical Research Communications 2008 375 623 627 10.1016/j.bbrc.2008.08.047 18722350
69. Detection of estradiol-17 during a mass coral spawn. S Atkinson M Atkinson, Coral Reefs 1992 11 33 5 10.1007/BF00291932
70. Effects of steroidal estrogens on coral growth and reproduction. A Tarrant M Atkinson S Atkinson, Marine Ecology Progress Series 2004 269 121 9 10.3354/meps269121
71. Immunohistochemical localization of a retinoic acid-like receptor in nerve cells of two colonial anthozoans (Cnidaria). M Bouzaiene A Angers M Anctil, Tissue and Cell 2007 39 123 130 10.1016/j.tice.2007.02.001 17376496
72. Nuclear receptors and lipid physiology: opening the X-files. A Chawla J Repa R Evans D Mangelsdorf, Science 2001 294 1866 70 10.1126/science.294.5548. 1866 11729302
73. The RXR heterodimers and orphan receptors. D Mangelsdorf R Evans, Cell 1995 83 841 50 10.1016/0092-8674(95)90200-7 8521508
74. A protein interaction atlas for the nuclear receptors: properties and quality of a hub-based dimerisation network. G Amoutzias E Pichler N Mian D De Graaf A Imsiridou M Robinson-Rechavi E Bornberg-Bauer D Robertson S Oliver, BMC Systems Biology 2007 1 34 10.1186/1752-0509-1-34 17672894
75. A map of the interactome network of the metazoan C. elegans. S Li CM Armstrong N Bertin H Ge S Milstein M Boxem P-O Vidalain J-DJ Han A Chesneau T Hao, et al. Science 2004 303 540 543 10.1126/science.1091403 14704431
76. Nuclear hormone receptors in C. elegans. A Antebi, Wormbook, The C. elegans Research Community 2006 http://www.wormbook.org doi/10.1895/wormbook.1. 64.1
77. Evolution by Gene Duplication. S Ohno, Heidelberg Springer-Verlag 1970
78. Evolution by gene duplication: an update. J Zhang, Trends in Ecology & Evolution 2003 18 292 298
79. Investigating the origins of triploblasty: 'mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). MQ Martindale K Pang JR Finnerty, Development 2004 131 2463 2474 15128674
80. Genomic organization, gene structure, and developmental expression of three Clustered otx genes in the sea anemone Nematostella vectensis. ME Mazza K Pang MQ Martindale JR Finnerty, Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2007 308B 494 506
81. Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission. AM Reitzel PM Burton C Krone JR Finnerty, Invertebrate Biology 2007 126 99 112
82. Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). J Fritzenwanker U Technau, Development, Genes and Evolution 2002 212 99 103
83. Differential gene expression in diapausing and active Calanus finmarchicus (Copepoda). A Tarrant M Baumgartner T Verslycke C Johnson, Marine Ecology Progress Series 2008 355 193 207
84. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. JW Thornton E Need D Crews, Science 2003 301 1714 1717 14500980
85. The first completed genome sequence from a teleost fish (Fugu rubripes) adds significant diversity to the nuclear receptor superfamily. JM Maglich JA Caravella MH Lambert TM Willson JT Moore L Ramamurthy, Nucl Acids Res 2003 31 4051 4058 12853622
86. Nuclear hormone receptor signaling in amphioxus. M Schubert F Brunet M Paris S Bertrand G Benoit V Laudet, Development Genes and Evolution 2008 218 651 665 18815806
87. MUSCLE: multiple sequence alignment with high accuracy and high throughput. R Edgar, Nucleic Acids Research 2004 32 1792 7 15034147
88. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. A Stamatakis, Bioinformatics 2006 22 2688 90 16928733
89. ProtTest: selection of best-fit models of protein evolution. F Abascal R Zardoya D Posada, Bioinformatics 2005 21 2104 5 15647292
90. GenePalette: a universal software tool for genome sequence visualization and analysis. M Rebeiz J Posakony, Developmental Biology 2004 271 431 8 15223345
91. Mfold web server for nucleic acid folding and hybridization prediction. M Zuker, Nucl Acids Res 2003 31 3406 3415 12824337
92. Estrogen receptor-related receptors in the killifish Fundulus heteroclitus: diversity, expression, and estrogen responsiveness. A Tarrant S Greytak G Callard M Hahn, Journal of Molecular Endocrinology 2006 37 105 20 16901928