Evolutionary genomics of nuclear receptors: From twenty-five ancestral genes to derived endocrine systems

Molecular Biology and Evolution

Volumn 21, Issue 10, 2004, Pages 1923-1937

  Bertrand, Stéphanie ^a   Brunet, Frédéric G ^a   Escriva, Hector ^a   Parmentier, Gilles ^a   Laudet, Vincent ^a   Robinson Rechavi, Marc ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bilaterian; Development; Endocrinology; Gene duplication; Gene loss; Phylogeny

Indexed keywords

CELL NUCLEUS RECEPTOR; HORMONE RECEPTOR; RETINOID; STEROID; THYROID HORMONE RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; ENDOCRINE SYSTEM; EVOLUTION; EXPRESSED SEQUENCE TAG; GENE DUPLICATION; GENE LOSS; GENE SEQUENCE; GENETIC VARIABILITY; GENOMICS; HOMEOSTASIS; METAZOON; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REGULATORY MECHANISM; URBILATERIA;

ANIMALS; ENDOCRINE SYSTEM; EVOLUTION, MOLECULAR; GENETIC MARKERS; INSECTS; LIKELIHOOD FUNCTIONS; MULTIGENE FAMILY; NEMATODA; PHYLOGENY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; UROCHORDATA; VERTEBRATES;

ANIMALIA; BILATERIA; METAZOA; NEMATODA; VERTEBRATA;

EID: 4944258189     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh200     Document Type: Article

References (80)

1. Aboobaker, A. A., and M. L. Blaxter. 2003. Hox gene loss during dynamic evolution of the nematode cluster. Curr. Biol. 13:37-40.
2. Adam, G., N. Perrimon, and S. Noselli. 2003. The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 130:2397-2406.
3. Adams, M. D., S. E. Celniker, R. A. Holt et al. (196 co-authors). 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
4. Adoutte, A., G. Balavoine, N. Lartillot, O. Lespinet, B. Prud'homme, and R. de Rosa. 2000. The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. USA 97:4453-4456.
5. Aguinaldo, A. M., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489-493.
6. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
7. Amores, A., A. Force, Y. L. Yan et al. (13 co-authors). 1998. Zebrafish Hox clusters and vertebrate genome evolution. Science 282:1711-1714.
8. Amores, A., T. Suzuki, Y.-L. Yan, J. Pomeroy, A. Singer, C. Amemiya, and J. H. Postlethwait. 2004. Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res. 14:1-10.
9. Auwerx, J., J. Drouin, and V. Laudet. 2003. Recepteurs a la Provencale. EMBO workshop on the biology of nuclear receptors. EMBO Rep. 4:1122-1126.
10. Baker, M. E. 2003. Evolution of adrenal and sex steroid action in vertebrates: a ligand-based mechanism for complexity. Bioessays 25:396-400.
11. Bardet, P. L., B. Horard, M. Robinson-Rechavi, V. Laudet, and J. M. Vanacker. 2002. Characterization of oestrogen receptors in zebrafish (Danio rerio). J. Mol. Endocrinol. 28:153-163.
12. Bardet, P. L., S. Obrecht-Pflumio, C. Thisse, V. Laudet, B. Thisse, and J. M. Vanacker. 2004. Cloning and developmental expression of five estrogen-receptor related (ERR) genes in the zebrafish. Dev. Genes. Evol. 214:240-249.
13. Blair, J. E., K. Ikeo, T. Gojobori, and S. B. Hedges. 2002. The evolutionary position of nematodes. BMC Evol. Biol. 2:7.
14. Bury, N. R., A. Sturm, P. Le Rouzic, C. Lethimonier, B. Ducouret, Y. Guiguen, M. Robinson-Rechavi, V. Laudet, M. E. Rafestin-Oblin, and P. Prunet. 2003. Evidence for two distinct functional glucocorticoid receptors in teleost fish. J. Mol. Endocrinol. 31:141-156.
15. Christoffels, A., E. G. L. Koh, J.-M. Chia, S. Brenner, S. Aparicio, and B. Venkatesh. 2004. Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol. Biol. Evol. 21: 1146-1151.
16. Clouse, S. D. 2002. Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol. Cell 10:973-982.
17. Dehal, P., Y. Satou, R. K. Campbell et al. (87 co-authors). 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157-2167.
18. Dopazo, H., J. Santoyo, and J. Dopazo. 2004. Phylogenomics and the number of characters required for obtaining an accurate phylogeny of eukaryote model species. Bioinformatics 20:i116-121.
19. Escriva, H., F. Delaunay, and V. Laudet. 2000. Ligand binding and nuclear receptor evolution. Bioessays 22:717-727.
20. Escriva, H., N. D. Holland, H. Gronemeyer, V. Laudet, and L. Z. Holland. 2002. The retinoic acid signaling pathway regulates anterior/posterior patterning in the nerve cord and pharynx of amphioxus, a chordate lacking neural crest. Development 129:2905-2916.
21. Escriva, H., V. Laudet, and M. Robinson-Rechavi. 2003. Nuclear receptors are markers of animal genome evolution. J. Struct. Funct. Genomics 3:177-184.
22. Escriva, H., R. Safi, C. Hänni, M.-C. Langlois, P. Saumitou-Laprade, D. Stehelin, A. Capron, R. Pierce, and V. Laudet. 1997. Ligand binding was aquired during evolution of nuclear receptors. Proc. Natl. Acad. Sci. USA 94:6803-6808.
23. Galtier, N., M. Gouy, and C. Gautier. 1996. SEA VIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
24. Gissendanner, C. R., K. Crossgrove, K. A. Kraus, C. V. Maina, and A. E. Sluder. 2004. Expression and function of conserved nuclear receptor genes in Caenorhabditis elegans. Dev. Biol. 266:399-416.
25. Grasso, L. C., D. C. Hayward, J. W. H. Trueman, K. M. Hardie, P. A. Janssens, and E. E. Ball. 2001. The evolution of nuclear receptors: evidence from the coral Acrospora. Mol. Phyl. Evol. 21:93-102.
26. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
27. Gustafsson, J. A. 1999. Seeking ligands for lonely orphan receptors. Science 284:1285-1286.
28. Holewa, B., D. Zapp, T. Drewes, S. Senkel, and G. U. Ryffel. 1997. HNF4beta, a new gene of the HNF4 family with distinct activation and expression profiles in oogenesis and embryogenesis of Xenopus laevis. Mol. Cell. Biol. 17:687-694.
29. Holland, L. Z., and J. J. Gibson-Brown. 2003. The Ciona intestinalis genome: when the constraints are off. Bioessays 25: 529-532.
30. Holland, P. W., J. Garcia-Fernandez, N. A. Williams, and A. Sidow. 1994. Gene duplications and the origins of vertebrate development. Development (Suppl.): 125-133.
31. Holt, R. A., G. M. Subramanian, A. Halpern et al. (123 co-authors). 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129-149.
32. Hughes, A. L., J. da Suva, and R. Friedman. 2001. Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res. 11:771-780.
33. Hughes, A. L., and R. Friedman. 2003. 2R or not 2R: testing hypotheses of genome duplication in early vertebrates. J. Struct. Funct. Genomics 3:85-93.
34. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
35. Kliewer, S. A., J. M. Lehmann, and T. M. Willson. 1999. Orphan nuclear receptors: shifting endocrinology into reverse. Science 284:757-760.
36. Krylov, D. M., Y. I. Wolf, I. B. Rogozin, and E. V. Koonin. 2003. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res. 13:2229-2235.
37. Laudet, V. 1997. Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J. Mol. Endocrinol. 19:207-226.
38. Laudet, V., and H. Gronemeyer. 2002. The nuclear receptors factsbook. Academic Press, London.
39. Laudet, V., C. Hänni, J. Coll, C. Catzeflis, and D. Stéhelin. 1992. Evolution of the nuclear receptor gene family. EMBO J. 11:1003-1013.
40. Lespinet, O., Y. I. Wolf, E. V. Koonin, and L. Aravind. 2002. The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res. 12:1048-1059.
41. Lynch, M., and J. S. Conery. 2003. The origins of genome complexity. Science 302:1401-1404.
42. Maglich, J. M., J. A. Caravella, M. H. Lambert, T. M. Willson, J. T. Moore, and L. Ramamurthy. 2003. The first completed genome sequence from a teleost fish (Fugu rubripes) adds significant diversity to the nuclear receptor superfamily. Nucleic Acids Res. 31:4051-4058.
43. Maglich, J. M., A. E. Sluder, X. Guan, Y. Shi, D. D. McKee, K. Carrick, K. Kamdar, T. M. Willson, and J. T. Moore. 2001. Comparison of complete nuclear receptor sets from the human, Caenorhabditis elegans and Drosophila genomes. GenomeBiology.com 2:research0029.0021-0029.0027.
44. Mallatt, J., and C. J. Winchell. 2002. Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol. Biol. Evol. 19:289-301.
45. Mansfield, S. G., S. Cammer, S. C. Alexander, D. P. Muehleisen, R. S. Gray, A. Tropsha, and W. E. Bollenbacher. 1998. Molecular cloning and characterization of an invertebrate cellular retinoic acid binding protein. Proc. Natl. Acad. Sci. USA 95:6825-6830.
46. Marchand, O., R. Safi, H. Escriva, E. Van Rompaey, P. Prunet, and V. Laudet. 2001. Molecular cloning and characterization of thyroid hormone receptors in teleost fish. J. Mol. Endocrinol. 21:51-65.
47. McLysaght, A., K. Hokamp, and K. H. Wolfe. 2002. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31:200-204.
48. Meyer, A., and M. Schartl. 1999. Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene fonctions. Curr. Opin. Cell Biol. 1:699-704.
49. Miyata, T., and H. Suga. 2001. Divergence pattern of animal gene families and relationship with the Cambrian explosion. Bioessays 23:1018-1027.
50. Nuclear Receptors Nomenclature Committee. 1999. A unified nomenclature system for the nuclear receptor superfamily. Cell 97:1-3.
51. Ono, K., H. Suga, N. Iwabe, K. Kuma, and T. Miyata. 1999. Multiple protein tyrosine phosphatases in sponges and explosive gene duplication in the early evolution of animals before the parazoan-eumetazoan split. J. Mol. Evol. 48: 654-662.
52. Ostberg, T., M. Jacobsson, A. Attersand, A. Mata de Urquiza, and L. Jendeberg. 2003. A triple mutant of the Drosophila ERR confers ligand-induced suppression of activity. Biochemistry 42:6427-6435.
53. Panopoulou, G., S. Hennig, D. Groth, A. Krause, A. J. Poustka, R. Herwig, M. Vingron, and H. Lehrach. 2003. New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. Genome Res. 13:1056-1066.
54. Postlethwait, J. H., I. G. Woods, P. Ngo-Hazelett, Y. L. Yan, P. D. Kelly, F. Chu, H. Huang, A. Hill-Force, and W. S. Talbot. 2000. Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 10:1890-1902.
55. Rat Genome Sequencing Project Consortium. 2004. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493-521.
56. Robinson-Rechavi, M., B. Boussau, and V. Laudet. 2004. Phylogenetic dating and characterization of gene duplications in vertebrates: the cartilaginous fish reference. Mol. Biol. Evol. 21:580-586.
57. Robinson-Rechavi, M., A.-S. Carpentier, M. Duffraisse, and V. Laudet. 2001a. How many nuclear hormone receptors in the human genome? Trends Genet. 17:554-556.
58. Robinson-Rechavi, M., and V. Laudet. 2003. Bioinformatics of nuclear receptors. Meth. Enz. 364:95-118.
59. Robinson-Rechavi, M., C. V. Maina, C. R. Gissendar, V. Laudet, and A. Sluder. 2004. Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. J. Mol. Evol. (in press).
60. Robinson-Rechavi, M., O. Marchand, H. Escriva, P.-L. Bardet, D. Zelus, S. Hughes, and V. Laudet. 2001b. Euteleost fish genomes are characterized by expansion of gene families. Genome Res. 11:781-788.
61. Robinson-Rechavi, M., O. Marchand, H. Escriva, and V. Laudet. 2001c. An ancestral whole-genome duplication may not have been responsible for the abundance of duplicated fish genes. Currt. Biol. 11:R458-R459.
62. Ruau, D., J. Duarte, T. Ourjdal, G. Perriere, V. Laudet, and M. Robinson-Rechavi. 2004. Update of Nurebase: nuclear hormone receptor functional genomics. Nucleic Acids Res. 32 (Database):D165-167.
63. Ruse, M. D., Jr., M. L. Privalsky, and F. M. Sladek. 2002. Competitive cofactor recruitment by orphan receptor hepatocyte nuclear factor 4alphal: modulation by the F domain. Mol. Cell. Biol. 22:1626-1638.
64. Saitou, N., and M. Nei. 1987. The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
65. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. Tree-Puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
66. Sengupta, P., H. A. Colbert, and C. I. Bargmann. 1994. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79:971-980.
67. Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114-1116.
68. Sluder, A. E., and C. V. Maina. 2001. Nuclear receptors in nematodes: themes and variations. Trends Genet. 17:206-213.
69. Sluder, A. E., S. W. Mathews, D. Hough, V. P. Yin, and C. V. Maina. 1999. The nuclear receptor superfamily has undergone extensive proliferation and diversification in nematodes. Genome Res. 9:103-120.
70. Stassen, M. J., D. Bailey, S. Nelson, V. Chinwalla, and P. J. Harte. 1995. The Drosophila trithorax proteins contain a novel variant of the nuclear receptor type DNA binding domain and an ancient conserved motif found in other chromosomal proteins. Mech. Dev. 52:209-223.
71. Stein, L. D., Z. Bao, D. Blasiar et al. (35 co-authors). 2003. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol. 1:166-192.
72. Suga, H., M. Koyanagi, D. Hoshiyama, K. Ono, N. Iwabe, K. Kuma, and T. Miyata. 1999. Extensive gene duplication in the early evolution of animals before the parazoaneumetazoan split demonstrated by G proteins and protein tyrosine kinases from sponge and hydra. J. Mol. Evol. 48:646-653.
73. Thomton, J. W., E. Need, and D. Crews. 2003. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714-1717.
74. Vandepoele, K., W. De Vos, J. S. Taylor, A. Meyer, and Y. Van De Peer. 2004. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc. Natl. Acad. Sci. USA 101:1638-1643.
75. Wang, Z., G. Benoit, J. Liu, S. Prasad, P. Aarnisalo, X. Liu, H. Xu, N. P. Walker, and T. Perlmann. 2003. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423:555-560.
76. Waterston, R. H., K. Lindblad-Toh, E. Birney et al. (222 co-authors). 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420:520-562.
77. Wiens, M., R. Batel, M. Korzhev, and W. E. G. Muller. 2003. Retinoid X receptor and retinoic acid response in the marine sponge Suberites domuncula. J. Exp. Biol. 206: 3261-3271.
78. Wolf, Y. I., I. B. Rogozin, and E. V. Koonin. 2004. Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. Genome Res. 14:29-36.
79. Yagi, K., Y. Satou, F. Mazet, S. M. Shimeld, B. Degnan, D. Rokhsar, M. Levine, Y. Kohara, and N. Satoh. 2003. A genome-wide survey of developmentally relevant genes in Ciona intestinalis. III. Genes for Fox, ETS, nuclear receptors and NFkappaB. Dev. Genes. Evol. 213:235-244.
80. Zhang, Z., P. E. Burch, A. J. Cooney, R. B. Lanz, F. A. Pereira, J. Wu, R. A. Gibbs, G. Weinstock, and D. A. Wheeler. 2004. Genomic analysis of the nuclear receptor family: new insights into structure, regulation, and evolution from the rat genome. Genome Res. 14:580-590.