Evolutionary history and functional characterization of androgen receptor genes in jawed vertebrates

Endocrinology

Volumn 150, Issue 12, 2009, Pages 5415-5427

  Ogino, Yukiko ^a   Katoh, Hironori ^a   Kuraku, Shigehiro ^b   Yamada, Gen ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR;

ACIPENSERIFORMES; ACTINOPTERYGII; ARTICLE; CHONDRICHTHYES; CHROMOSOME 10; CHROMOSOME 14; FISH; GENE DUPLICATION; GENE FUNCTION; GENETIC ANALYSIS; GENOME; HUMAN; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEICHTHYES; OSTEOGLOSSIFORMES; PHYLOGENY; PRIORITY JOURNAL; SHARK; TELEOST; VERTEBRATE;

ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; CHROMOSOME MAPPING; COS CELLS; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; FISH PROTEINS; FISHES; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; ORYZIAS; PHYLOGENY; RECEPTORS, ANDROGEN; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, DNA; SHARKS; TRANSFECTION; VERTEBRATES;

EID: 71949095895     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-0523     Document Type: Article

References (92)

1. Behringer RR, Eakin GS, Renfree MB 2006 Mammalian diversity: gametes, embryos and reproduction. Reprod Fertil Dev 18:99-107
2. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM 1995 The nuclear receptor superfamily: the second decade. Cell 83: 835-839 (Pubitemid 126663112)
3. Baker ME 1997 Steroid receptor phylogeny and vertebrate origins. Mol Cell Endocrinol 135:101-107
4. Laudet V 1997 Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J Mol Endocrinol 19:207-226 (Pubitemid 28023157)
5. Thornton JW, Kelley DB 1998 Evolution of the androgen receptor: structure-function implications. Bioessays 20:860-869 (Pubitemid 28486023)
6. Escriva H, Delaunay F, Laudet V 2000 Ligand binding and nuclear receptor evolution. Bioessays 22:717-727 (Pubitemid 30613303)
7. Escriva H, Safi R, Hänni C, Langlois MC, Saumitou-Laprade P, Stehelin D, Capron A, Pierce R, Laudet V 1997 Ligand binding was acquired during evolution of nuclear receptors. Proc Natl Acad Sci USA 94:6803-6808 (Pubitemid 27281945)
8. Baker ME 2001 Adrenal and sex steroid receptor evolution: environmental implications. J Mol Endocrinol 26:119-125
9. Thornton JW 2001 Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci USA 98:5671-5676
10. Baker ME 2002 Albumin, steroid hormones and the origin of vertebrates. J Endocrinol 175:121-127
11. Bridgham JT, Carroll SM, Thornton JW 2006 Evolution of hormone- receptor complexity by molecular exploitation. Science 312: 97-101
12. Paris M, Pettersson K, Schubert M, Bertrand S, Pongratz I, Escriva H, Laudet V 2008 An amphioxus orthologue of the estrogen receptor that does not bind estradiol: insights into estrogen receptor evolution. BMC Evol Biol 8:219
13. Todo T, Ikeuchi T, Kobayashi T, Nagahama Y 1999 Fish androgen receptor: cDNA cloning, steroid activation of transcription in transfected mammalian cells, and tissue mRNA levels. Biochem Biophys Res Commun 254:378-383 (Pubitemid 29290408)
14. Ikeuchi T, Todo T, Kobayashi T, Nagahama Y 1999 cDNA cloning of a novel androgen receptor subtype. J Biol Chem 274:25205-25209 (Pubitemid 129530680)
15. Sperry TS, Thomas P 1999 Characterization of two nuclear androgen receptors in Atlantic croaker: comparison of their biochemical properties and binding specificities. Endocrinology 140:1602-1611
16. Takeo J, Yamashita S 1999 Two distinct isoforms of cDNA encoding rainbow trout androgen receptors. J Biol Chem 274:5674-5680 (Pubitemid 29109220)
17. Borg B 1994 Androgens in teleost fishes. Comp Biochem Physiol 109C:219-245
18. Ogino Y, Katoh H, Yamada G 2004 Androgen dependent development of a modified anal fin, gonopodium, as a model to understand the mechanism of secondary sexual character expression in vertebrates. FEBS Lett 575:119-126 (Pubitemid 39237692)
19. Wittbrodt J, Meyer A, Schartl M 1998 More genes in fish? Bioessays 20:511-515
20. Hoegg S, Brinkmann H, Taylor JS, Meyer A 2004 Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190-203 (Pubitemid 39128342)
21. Douard V, Brunet F, Boussau B, Ahrens-Fath I, Vlaeminck-Guillem V, Haendler B, Laudet V, Guiguen Y 2008 The fate of the duplicated androgen receptor in fishes: a late neofunctionalization event?BMC Evol Biol 8:336
22. Venkatesh B, Kirkness EF, Loh YH, Halpern AL, Lee AP, Johnson J, Dandona N, Viswanathan LD, Tay A, Venter JC, Strausberg RL, Brenner S 2007 Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol 5:e101
23. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y, Jindo T, Kobayashi D, Shimada A, Toyoda A, Kuroki Y, Fujiyama A, Sasaki T, Shimizu A, Asakawa S, Shimizu N, Hashimoto S, Yang J, Lee Y, Matsushima K, Sugano S, et al. 2007 The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714-719 (Pubitemid 46889726)
24. Leihy MW, Shaw G, Wilson JD, Renfree MB 2004 Penile development is initiated in the tammar wallaby pouch young during the period when 5α-androstane-3α,17β-diol is secreted by the testes. Endocrinology 145:3346-3352 (Pubitemid 38832528)
25. Quigley CA, De Bellis A, Marschke KB, el-Awady MK, Wilson EM, French FS 1995 Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 16:271-321
26. Bryan MB, Scott AP, Li W 2007 The sea lamprey (Petromyzon marinus) has a receptor for androstenedione. Biol Reprod 77:688-696
27. Saitou N, Nei M 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
28. Katoh K, Kuma K, Toh H, Miyata T 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511-518 (Pubitemid 40360980)
29. Guindon S, Gascuel O 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704 (Pubitemid 37365050)
30. Felsenstein J 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
31. Ronquist F, Huelsenbeck JP 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574 (Pubitemid 37038874)
32. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402 (Pubitemid 27359211)
33. Turner DL, Weintraub H 1994 Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8:1434-1447
34. Rupp RA, Snider L, Weintraub H 1994 Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev 8:1311-1323 (Pubitemid 24181322)
35. Katoh H, Ogino Y, Yamada G 2006 Cloning and expression analysis of androgen receptor gene in chicken embryogenesis. FEBS Lett 580:1607-1615 (Pubitemid 43290359)
36. Matsui D, Sakari M, Sato T, Murayama A, Takada I, Kim M, Takeyama K, Kato S 2002 Transcriptional regulation of the mouse steroid 5α-reductase type II gene by progesterone in brain. Nucleic Acids Res 30:1387-1393 (Pubitemid 34679717)
37. Kinoshita M, Ozato K 1995 Cytoplasmic microinjection of DNA into fertilized medaka (Oryzias latipes) eggs. Fish Biol J Medaka 7:59-64
38. Krust A, Green S, Argos P, Kumar V, Walter P, Bornert JM, Chambon P 1986 The chicken oestrogen receptor sequence: homology with v-erbA and the human oestrogen and glucocorticoid receptors. EMBO J 5:891-897
39. Scheidereit C, Westphal HM, Carlson C, Bosshard H, Beato M 1986 Molecular model of the interaction between the glucocorticoid receptor and the regulatory elements of inducible genes. DNA 5:383-391 (Pubitemid 17188092)
40. Strähle U, Klock G, Schütz G 1987 ADNA sequence of 15 base pairs is sufficient to mediate both glucocorticoid and progesterone induction of gene expression. Proc Natl Acad Sci USA 84:7871-7875 (Pubitemid 17162809)
41. Ham J, Thomson A, Needham M, Webb P, Parker M 1988 Characterization of response elements for androgens, glucocorticoids and progestins in mouse mammary tumour virus. Nucleic Acids Res 16:5263-5276 (Pubitemid 18163282)
42. Umesono K, Evans RM 1989 Determinants of target gene specificity for steroid/thyroid hormone receptors. Cell 57:1139-1146 (Pubitemid 19169810)
43. Sack JS, Kish KF, Wang C, Attar RM, Kiefer SE, An Y, Wu GY, Scheffler JE, Salvati ME, Krystek Jr SR, Weinmann R, Einspahr HM 2001 Crystallographic structures of the ligand-binding domains of the androgen receptor and its T877A mutant complexed with the natural agonist dihydrotestosterone. Proc Natl Acad Sci USA 98: 4904-4909 (Pubitemid 32397055)
44. 2-terminal conserved motif interacts with the COOH terminus of the Hsp70-interacting protein (CHIP). J Biol Chem 279:30643-30653
45. 2-/ carboxyl-terminal interactions in androgen receptor dimerization revealed by mutations that cause androgen insensitivity. J Biol Chem 273:92-101
46. 2-terminal interaction with the ligand binding domain of the androgen receptor. J Biol Chem 275:22986-22994
47. Hur E, Pfaff SJ, Payne ES, Grøn H, Buehrer BM, Fletterick RJ 2004 Recognition and accommodation at the androgen receptor coactivator binding interface. PLoS Biol 2:E274 (Pubitemid 39245241)
48. Thompson J, Saatcioglu F, Jänne OA, Palvimo JJ 2001 Disrupted amino- and carboxyl-terminal interactions of the androgen receptor are linked to androgen insensitivity. Mol Endocrinol 15:923-935 (Pubitemid 32510639)
49. Ghali SA, Gottlieb B, Lumbroso R, Beitel LK, Elhaji Y, Wu J, Pinsky L, Trifiro MA 2003 The use of androgen receptor amino/carboxylterminal interaction assays to investigate androgen receptor gene mutations in subjects with varying degrees of androgen insensitivity. J Clin Endocrinol Metab 88:2185-2193 (Pubitemid 36549896)
50. Jääskelainen J, Deeb A, Schwabe JW, Mongan NP, Martin H, Hughes IA 2006 Human androgen receptor gene ligand-bindingdomain mutations leading to disrupted interaction between the N-and C-terminal domains. J Mol Endocrinol 36:361-368
51. Savory JG, Préfontaine GG, Lamprecht C, Liao M, Walther RF, Lefebvre YA, Haché RJ 2001 Glucocorticoid receptor homodimers and glucocorticoid-mineralocorticoid receptor heterodimers form in the cytoplasm through alternative dimerization interfaces. Mol Cell Biol 21:781-793
52. Fawell SE, Lees JA, White R, Parker MG 1990 Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell 60:953-962 (Pubitemid 20103877)
53. Bledsoe RK, Montana VG, Stanley TB, Delves CJ, Apolito CJ, McKee DD, Consler TG, Parks DJ, Stewart EL, Willson TM, Lambert MH, Moore JT, Pearce KH, Xu HE 2002 Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 110:93-105
54. Williams SP, Sigler PB 1998 Atomic structure of progesterone complexed with its receptor. Nature 393:392-396 (Pubitemid 28269716)
55. Nemoto T, Ohara-Nemoto Y, Shimazaki S, Ota M 1994 Dimerization characteristics of the DNA- and steroid-binding domains of the androgen receptor. J Steroid Biochem Mol Biol 50:225-233 (Pubitemid 24309114)
56. Miura T, Yamauchi K, Takahashi H, Nagahama Y 1991 Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc Natl Acad Sci USA 88:5774-5778
57. Barannikova IA, Dyubin VP, Bayunova LV, Semenkova TB 2002 Steroids in control of reproductive function in fish. Neurosci Behav Physiol 32:141-148
58. Georget V, Lobaccaro JM, Terouanne B, Mangeat P, Nicolas JC, Sultan C 1997 Trafficking of the androgen receptor in living cells with fused green fluorescent protein-androgen receptor. Mol Cell Endocrinol 129:17-26 (Pubitemid 27229213)
59. Simental JA, Sar M, Lane MV, French FS, Wilson EM 1991 Transcriptional activation and nuclear targeting signals of the human androgen receptor. J Biol Chem 266:510-518 (Pubitemid 21906153)
60. Roy AK, Tyagi RK, Song CS, Lavrovsky Y, Ahn SC, Oh TS, Chatterjee B 2001 Androgen receptor: structural domains and functional dynamics after ligand-receptor interaction. Ann NY Acad Sci 949:44-57 (Pubitemid 34059960)
61. Jenster G, Trapman J, Brinkmann AO 1993 Nuclear import of the human androgen receptor. Biochem J 293(Pt 3):761-768 (Pubitemid 23244561)
62. 2-terminal and carboxyl-terminal sequences. J Biol Chem 269:13115-13123
63. Picard D, Yamamoto KR 1987 Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J 6:3333-3340
64. Chopin-Delannoy S, Thénot S, Delaunay F, Buisine E, Begue A, Duterque-Coquillaud M, Laudet V 2003 A specific and unusual nuclear localization signal in the DNA binding domain of the Reverb orphan receptors. J Mol Endocrinol 30:197-211 (Pubitemid 36592513)
65. Black BE, Holaska JM, Rastinejad F, Paschal BM 2001 DNA binding domains in diverse nuclear receptors function as nuclear export signals. Curr Biol 11:1749-1758 (Pubitemid 33098556)
66. Saporita AJ, Zhang Q, Navai N, Dincer Z, Hahn J, Cai X, Wang Z 2003 Identification and characterization of a ligand-regulated nuclear export signal in androgen receptor. J Biol Chem 278:41998-42005 (Pubitemid 37310463)
67. Kumar S, Hedges SB 1998 A molecular timescale for vertebrate evolution. Nature 392:917-920
68. Garnier DH, Sourdaine P, Jégou B 1999 Seasonal variations in sex steroids and male sexual characteristics in Scyliorhinus canicula. Gen Comp Endocrinol 116:281-290
69. Cuevas ME, Callard G 1992 Androgen and progesterone receptors in shark (Squalus) testis: characteristics and stage-related distribution. Endocrinology 130:2173-2182
70. Bryan MB, Scott AP, LiW 2008 Sex steroids and their receptors in lampreys. Steroids 73:1-12
71. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH 1998 Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711-1714 (Pubitemid 28549287)
72. Amores A, Suzuki T, Yan YL, Pomeroy J, Singer A, Amemiya C, Postlethwait JH 2004 Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res 14:1-10 (Pubitemid 38088519)
73. Meyer A, Schartl M 1999 Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699-704
74. Taylor JS, Van de Peer Y, Braasch I, Meyer A 2001 Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc Lond B Biol Sci 356:1661-1679 (Pubitemid 32996721)
75. Taylor JS, Van de Peer Y, Meyer A 2001 Revisiting recent challenges to the ancient fish-specific genome duplication hypothesis. Curr Biol 11:R1005-R1008 (Pubitemid 33146405)
76. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y 2003 Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382-390 (Pubitemid 36395395)
77. Van de Peer Y, Frickey T, Taylor J, Meyer A 2002 Dealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genes. Gene 295:205-211 (Pubitemid 35279252)
78. Kuraku S, Meyer A 2009 The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. Int J Dev Biol 53:765-773
79. Volff JN 2005 Genome evolution and biodiversity in teleost fish. Heredity 94:280-294
80. Escrivá García H, Laudet V, Robinson-Rechavi M 2003 Nuclear receptors are markers of animal genome evolution. J Struct Funct Genomics 3:177-184 (Pubitemid 36460255)
81. Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan YL, Kelly PD, Chu F, Huang H, Hill-Force A, Talbot WS 2000 Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res 10:1890-1902 (Pubitemid 32049135)
82. Graham A, Papalopulu N, Krumlauf R 1989 The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57:367-378
83. Garcia-Fernández J, Holland PW 1994 Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563-566 (Pubitemid 24264923)
84. Allendorf FW, Thorgaard GH 1984 Tetraploidy and the evolution of Salmonid fishes. Evolutionary genetics of fishes. New York: Plenum Publishing Corp.; 1-53
85. Cresko WA, Yan YL, Baltrus DA, Amores A, Singer A, Rodríguez- Marí A, Postlethwait JH 2003 Genome duplication, subfunction partitioning, and lineage divergence: Sox9 in stickleback and zebrafish. Dev Dyn 228:480-489 (Pubitemid 37372769)
86. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biémont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigó R, Zody MC, Mesirov J, Lindblad- Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quétier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H 2004 Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946-957
87. Ohno S 1970 Evolution of gene duplication. New York: Springer Verlag
88. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA 1997 Mouse estrogen receptor β forms estrogen response element-binding heterodimers with estrogen receptor α. Mol Endocrinol 11:1486-1496 (Pubitemid 27366759)
89. Tremblay GB, Tremblay A, Labrie F, Giguère V 1999 Dominant activity of activation function 1 (AF-1) and differential stoichiometric requirements for AF-1 and -2 in the estrogen receptor α-β heterodimeric complex. Mol Cell Biol 19:1919-1927 (Pubitemid 29098250)
90. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J 1999 Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545 (Pubitemid 29177561)
91. Schmidt HA, Strimmer K, Vingron M, von Haeseler A 2002 TREE-PUZZLE: maximumlikelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502-504 (Pubitemid 34284960)
92. Azuma Y, Kumazawa Y, Miya M, Mabuchi K, Nishida M 2008 Mitogenomic evaluation of the historical biogeography of cichlids toward reliable dating of teleostean divergences. BMC Evol Biol 8:215