Molecular adaptation and resilience of the insect's nuclear receptor USP

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Chaumot, Arnaud ^b   Da Lage, Jean Luc ^c   Maestro, Oscar ^d   Martin, David ^d   Iwema, Thomas ^e   Brunet, Frederic ^a   Belles, Xavier ^d   Laudet, Vincent ^a   Bonneton, François ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UR MALY   (France)

^c CNRS   (France)

^d INSTITUTE OF EVOLUTIONARY BIOLOGY CSIC UNIVERSITAT POMPEU FABRA   (Spain)

^e UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

Ecdysone receptor; ECR; Mecopterida; Nuclear receptors; Selection; USP

Indexed keywords

BEETLE; COCKROACH; DIVERGENCE; EMERGENCE; FLY; LIGAND; MAXIMUM LIKELIHOOD ANALYSIS; MOLECULAR ANALYSIS; NATURAL SELECTION; PHENOTYPIC PLASTICITY; PROTEIN;

AMPHIESMENOPTERA; BLATTARIA; DIPTERA; DROSOPHILIDAE; HEXAPODA; LEPIDOPTERA; MECOPTERA; SIPHONAPTERA (FLEAS); TENEBRIONIDAE; TRICHOPTERA;

CELL RECEPTOR; ECDYSONE RECEPTOR; STEROID RECEPTOR;

ANIMAL; ARTICLE; BEETLE; CHEMICAL STRUCTURE; CHEMISTRY; COCKROACH; DROSOPHILIDAE; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BEETLES; COCKROACHES; DROSOPHILIDAE; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID;

EID: 84871257457     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-199     Document Type: Article

References (74)

1. Robustness, evolvability, and neutrality. Wagner A, FEBS Lett 2005 579 8 1772 1778 10.1016/j.febslet.2005.01.063 15763550 (Pubitemid 40342652)
2. The ecdysteroid receptor. Henrich VC, Comprehensive Molecular Insect Science Oxford: Elsevier, Gilbert LI, Iatrou K, Gill SS, 2005 243 285 vol. 3
3. Ecdysteroid hormone action. Spindler KD, Honl C, Tremmel C, Braun S, Ruff H, Spindler-Barth M, Cell Mol Life Sci 2009 66 24 3837 3850 10.1007/s00018-009-0112-5 19669094
4. Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR. Bonneton F, Zelus D, Iwema T, Robinson-Rechavi M, Laudet V, Mol Biol Evol 2003 20 4 541 553 10.1093/molbev/msg054 12654933 (Pubitemid 36437904)
5. The rapid divergence of the ecdysone receptor is a synapomorphy for Mecopterida that clarifies the Strepsiptera problem. Bonneton F, Brunet FG, Kathirithamby J, Laudet V, Insect Mol Biol 2006 15 3 351 362 10.1111/j.1365-2583.2006.00654.x 16756554 (Pubitemid 43821208)
6. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Bonneton F, Chaumot A, Laudet V, Insect Biochem Mol Biol 2008 38 4 416 429 10.1016/j.ibmb.2007.10.006 18342247
7. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. Iwema T, Billas IM, Beck Y, Bonneton F, Nierengarten H, Chaumot A, Richards G, Laudet V, Moras D, EMBO J 2007 26 16 3770 3782 10.1038/sj.emboj.7601810 17673910 (Pubitemid 47295877)
8. Structural and Evolutionary Innovation of the Heterodimerization Interface between USP and the Ecdysone Receptor ECR in Insects. Iwema T, Chaumot A, Studer RA, Robinson-Rechavi M, Billas IML, Moras D, Laudet V, Bonneton F, Mol Biol Evol 2009 26 4 753 768 10.1093/molbev/msn302 19126866
9. Heterotachy and functional shift in protein evolution. Philippe H, Casane D, Gribaldo S, Lopez P, Meunier J, IUBMB Life 2003 55 4-5 257 265 12880207 (Pubitemid 36842257)
10. The quest for natural selection in the age of comparative genomics. Anisimova M, Liberles DA, Heredity 2007 99 6 567 579 10.1038/sj.hdy.6801052 17848974 (Pubitemid 350146925)
11. Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Hughes AL, Heredity 2007 99 4 364 373 10.1038/sj.hdy.6801031 17622265 (Pubitemid 47482647)
12. Evidence for an episodic model of protein sequence evolution. Studer RA, Robinson-Rechavi M, Biochem Soc Trans 2009 37 Pt 4 783 786 19614594
13. Pervasive positive selection on duplicated and nonduplicated vertebrate protein coding genes. Studer RA, Penel S, Duret L, Robinson-Rechavi M, Genome Res 2008 18 9 1393 1402 10.1101/gr.076992.108 18562677
14. Mutation rate variation in multicellular eukaryotes: causes and consequences. Baer CF, Miyamoto MM, Denver DR, Nat Rev Genet 2007 8 8 619 631 10.1038/nrg2158 17637734 (Pubitemid 47077282)
15. Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Galtier N, Duret L, Trends Genet 2007 23 6 273 277 10.1016/j.tig.2007.03.011 17418442 (Pubitemid 46770896)
16. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Tamura K, Subramanian S, Kumar S, Mol Biol Evol 2004 21 1 36 44 12949132 (Pubitemid 38233516)
17. Relationships among pest flour beetles of the genus Tribolium (Tenebrionidae) inferred from multiple molecular markers. Angelini DR, Jockusch EL, Mol Phylogenet Evol 2008 46 1 127 141 10.1016/j.ympev.2007.08.017 18024090 (Pubitemid 350267216)
18. The phylogeny of cockroach families: is the current molecular hypothesis robust? Grandcolas P, D'haese C, Cladistics-the Int J Willi Hennig Soc 2001 17 1 48 55 10.1111/j.1096-0031.2001.tb00110.x (Pubitemid 32430570)
19. Evolution and phylogenetic information content of the ribosomal DNA repeat unit in the Blattodea (Insecta). Mukha D, Wiegmann BM, Schal C, Insect Biochem Mol Biol 2002 32 9 951 960 10.1016/S0965-1748(01)00164-3 12213231 (Pubitemid 35025328)
20. An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Gaunt MW, Miles MA, Mol Biol Evol 2002 19 5 748 761 10.1093/oxfordjournals.molbev.a004133 11961108 (Pubitemid 34521306)
21. PAML: a program package for phylogenetic analysis by maximum likelihood. Yang Z, Comput Appl Biosci 1997 13 5 555 556 9367129 (Pubitemid 27480216)
22. Statistical methods for detecting molecular adaptation. Yang Z, Bielawski JP, Trends Ecol Evol 2000 15 12 496 503 10.1016/S0169-5347(00)01994-7 11114436
23. A novel role for helix 12 of retinoid X receptor in regulating repression. Zhang J, Hu X, Lazar MA, Mol Cell Biol 1999 19 9 6448 6457 10454590 (Pubitemid 29399348)
24. TR surfaces and conformations required to bind nuclear receptor corepressor. Marimuthu A, Feng W, Tagami T, Nguyen H, Jameson JL, Fletterick RJ, Baxter JD, West BL, Mol Endocrinol 2002 16 2 271 286 10.1210/me.16.2.271 11818500 (Pubitemid 34131225)
25. Crystal structure of the ligand-binding domain of the ultraspiracle protein USP, the ortholog of retinoid X receptors in insects. Billas IML, Moulinier L, Rochel N, Moras D, J Biol Chem 2001 276 10 7465 7474 10.1074/jbc.M008926200 11053444
26. The structure of the ultraspiracle ligand-binding domain reveals a nuclear receptor locked in an inactive conformation. Clayton GM, Peak-Chew SY, Evans RM, Schwabe JW, Proc Natl Acad Sci U S A 2001 98 4 1549 1554 10.1073/pnas.98.4.1549 11171988 (Pubitemid 32165536)
27. Transcription activation by the ecdysone receptor (EcR/USP): identification of activation functions. Hu X, Cherbas L, Cherbas P, Mol Endocrinol 2003 17 4 716 731 10.1210/me.2002-0287 12554759 (Pubitemid 36403582)
28. The X-ray structure of a hemipteran ecdysone receptor ligand-binding domain-Comparison with a Lepidopteran ecdysone receptor ligand-binding domain and implications for insecticide design. Carmichael JA, Lawrence MC, Graham LD, Pilling PA, Epa VC, Noyce L, Lovrecz G, Winkler DA, Pawlak-Skrzecz A, Eaton RE, et al. J Biol Chem 2005 280 23 22258 22269 10.1074/jbc.M500661200 15809296 (Pubitemid 40827882)
29. Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Billas IM, Iwema T, Garnier JM, Mitschler A, Rochel N, Moras D, Nature 2003 426 6962 91 96 10.1038/nature02112 14595375 (Pubitemid 37432547)
30. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Zhang J, Nielsen R, Yang Z, Mol Biol Evol 2005 22 12 2472 2479 10.1093/molbev/msi237 16107592 (Pubitemid 41661383)
31. The role of GC-biased gene conversion in shaping the fastest evolving regions of the human genome. Kostka D, Hubisz MJ, Siepel A, Pollard KS, Mol Biol Evol 2012 29 3 1047 1057 10.1093/molbev/msr279 22075116
32. Diagnosing mitochondrial DNA diversity: applications of a sentinel gene approach. Clare EL, Kerr KC, von Konigslow TE, Wilson JJ, Hebert PD, J Mol Evol 2008 66 4 362 367 10.1007/s00239-008-9088-2 18368433
33. Evolutionary selection across the nuclear hormone receptor superfamily with a focus on the NR1I subfamily (vitamin D, pregnane X, and constitutive androstane receptors). Krasowski MD, Yasuda K, Hagey LR, Schuetz EG, Nucl Recept 2005 3 2 10.1186/1478-1336-3-2 16197547 (Pubitemid 41522382)
34. Adaptive evolution of the Retinoid X receptor in vertebrates. Philip S, Castro LF, da Fonseca RR, Reis-Henriques MA, Vasconcelos V, Santos MM, Antunes A, Genomics 2012 99 81 89 10.1016/j.ygeno.2011.12.001 22193333
35. Genomic analysis of the nuclear receptor family: new insights into structure, regulation, and evolution from the rat genome. Zhang Z, Burch PE, Cooney AJ, Lanz RB, Pereira FA, Wu J, Gibbs RA, Weinstock G, Wheeler DA, Genome Res 2004 14 4 580 590 10.1101/gr.2160004 15059999 (Pubitemid 38500229)
36. An integrated view of protein evolution. Pal C, Papp B, Lercher MJ, Nat Rev Genet 2006 7 5 337 348 10.1038/nrg1838 16619049
37. Controlling nuclear receptors: the circular logic of cofactor cycles. Perissi V, Rosenfeld MG, Nat Rev Mol Cell Biol 2005 6 7 542 554 10.1038/nrm1680 15957004 (Pubitemid 40943045)
38. Evolutionary identification of a subtype specific functional site in the ligand binding domain of steroid receptors. Raviscioni M, He Q, Salicru EM, Smith CL, Lichtarge O, Proteins 2006 64 4 1046 1057 10.1002/prot.21074 16835908 (Pubitemid 44420943)
39. Locust retinoid X receptors: 9-Cis-retinoic acid in embryos from a primitive insect. Nowickyj SM, Chithalen JV, Cameron D, Tyshenko MG, Petkovich M, Wyatt GR, Jones G, Walker VK, Proc Natl Acad Sci U S A 2008 105 28 9540 9545 10.1073/pnas.0712132105 18606996 (Pubitemid 352031337)
40. Small molecule pharmacological chaperones: From thermodynamic stabilization to pharmaceutical drugs. Arakawa T, Ejima D, Kita Y, Tsumoto K, Biochim Biophys Acta 2006 1764 11 1677 1687 10.1016/j.bbapap.2006.08.012 17046342 (Pubitemid 46053854)
41. Evolutionary constraint networks in ligand-binding domains: an information-theoretic approach. Nagl SB, Freeman J, Smith TF, Pac Symp Biocomput 1999 4 90 101
42. Effects of the structures of ecdysone receptor (EcR) and ultraspiracle (USP) on the ligand-binding activity of the EcR/USP heterodimer. Minakuchi C, Ogura T, Miyagawa H, Nakagawa Y, J Pestic Sci 2007 32 4 379 384 10.1584/jpestics.G07-19 (Pubitemid 350206959)
43. Molecular cloning of the ecdysone receptor and the retinoid X receptor from the scorpion Liocheles australasiae. Nakagawa Y, Sakai A, Magata F, Ogura T, Miyashita M, Miyagawa H, Febs J 2007 274 23 6191 6203 10.1111/j.1742-4658. 2007.06139.x 18028192 (Pubitemid 350135338)
44. Molecular cloning, expression analysis and functional confirmation of ecdysone receptor and ultraspiracle from the Colorado potato beetle Leptinotarsa decemlineata. Ogura T, Minakuchi C, Nakagawa Y, Smagghe G, Miyagawa H, Febs Journal 2005 272 16 4114 4128 10.1111/j.1742-4658.2005.04823.x 16098194 (Pubitemid 41160919)
45. The ecdysteroid receptor. Henrich VC, Insect endocrinology Amsterdam, Boston: Academic Press, Elsevier, Gilbert LI, 2012 177 218
46. Coexpression of nuclear receptor partners increases their solubility and biological activities. Li C, Schwabe JWR, Banayo E, Evans RM, Proc Natl Acad Sci U S A 1997 94 6 2278 2283 10.1073/pnas.94.6.2278 9122185 (Pubitemid 27136865)
47. Purification and characterization of recombinant ligand-binding domains from the ecdysone receptors of four pest insects. Graham LD, Pilling PA, Eaton RE, Gorman JJ, Braybrook C, Hannan GN, Pawlak-Skrzecz A, Noyce L, Lovrecz GO, Lu L, et al. Protein Expr Purif 2007 53 2 309 324 10.1016/j.pep.2006.12.011 17275327 (Pubitemid 46453202)
48. Ligand-induced heterodimerization between the ligand binding domains of the Drosophila ecdysteroid receptor and ultraspiracle. Lezzi M, Bergman T, Henrich VC, Vogtli M, Fromel C, Grebe M, Przibilla S, Spindler-Barth M, Eur J Biochem 2002 269 13 3237 3245 10.1046/j.1432-1033.2002.03001.x 12084064 (Pubitemid 34748110)
49. Separation of retinoid X receptor homo- and heterodimerization functions. Vivat-Hannah V, Bourguet W, Gottardis M, Gronemeyer H, Mol Cell Biol 2003 23 21 7678 7688 10.1128/MCB.23.21.7678-7688.2003 14560013 (Pubitemid 37271466)
50. Molecular evolution of ultraspiracle protein (USP/RXR) in insects. Hult EF, Tobe SS, Chang BS, PLoS One 2011 6 8 23416 10.1371/journal.pone.0023416 21901121
51. Molecular drive. Dover GA, Strachan T, Coen ES, Brown SD, Science 1982 218 4577 1069 7146895
52. Evolution of genetic redundancy for advanced players. Dover GA, Curr Opin Genet Dev 1993 3 6 902 910 10.1016/0959-437X(93)90012-E 8118216 (Pubitemid 24009896)
53. Evolution of the pregnane x receptor: adaptation to cross-species differences in biliary bile salts. Krasowski MD, Yasuda K, Hagey LR, Schuetz EG, Mol Endocrinol 2005 19 7 1720 1739 10.1210/me.2004-0427 15718292 (Pubitemid 41007886)
54. Computational study of evolutionary selection pressure on rainbow trout estrogen receptors. Shyu C, Brown CJ, Ytreberg FM, PLoS One 2010 5 3 9392 10.1371/journal.pone.0009392 20231885
55. Evolution of promiscuous nuclear hormone receptors: LXR, FXR, VDR, PXR, and CAR. Krasowski MD, Ni A, Hagey LR, Ekins S, Mol Cell Endocrinol 2011 334 1-2 39 48 20615451
56. An evolutionary analysis of orphan genes in Drosophila. Domazet-Loso T, Tautz D, Genome Res 2003 13 10 2213 2219 10.1101/gr.1311003 14525923 (Pubitemid 37265985)
57. Genome-wide acceleration of protein evolution in flies (Diptera). Savard J, Tautz D, Lercher MJ, BMC Evol Biol 2006 6 7 10.1186/1471-2148-6-7 16436210 (Pubitemid 43275531)
58. Evolution of nuclear receptors in insects. Bonneton F, Laudet V, Insect endocrinology Amsterdam, Boston: Academic Press; Elsevier, Gilbert LI, 2012 219
59. Dobzhansky-Muller incompatibilities in protein evolution. Kondrashov AS, Sunyaev S, Kondrashov FA, Proc Natl Acad Sci U S A 2002 99 23 14878 14883 10.1073/pnas.232565499 12403824 (Pubitemid 35334577)
60. Single fly DNA preps for PCR. Gloor G, Engels W, Drosophila Information Service 1992 71 148 149
61. Evolution of genes and genomes on the Drosophila phylogeny. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, et al. Nature 2007 450 7167 203 218 10.1038/nature06341 17994087
62. Quantity does matter. Juvenile hormone and the onset of vitellogenesis in the German cockroach. Cruz J, Martin D, Pascual N, Maestro JL, Piulachs MD, Belles X, Insect Biochem Mol Biol 2003 33 12 1219 1225 10.1016/j.ibmb.2003.06. 004 14599494 (Pubitemid 37488860)
63. PAML 4: phylogenetic analysis by maximum likelihood. Yang Z, Mol Biol Evol 2007 24 8 1586 1591 10.1093/molbev/msm088 17483113 (Pubitemid 47236688)
64. SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Galtier N, Gouy M, Gautier C, Comput Appl Biosci 1996 12 6 543 548 9021275
65. Congruence and controversy: toward a higher-level phylogeny of Diptera. Yeates DK, Wiegmann BM, Annu Rev Entomol 1999 44 397 428 10.1146/annurev.ento. 44.1.397 15012378 (Pubitemid 29096978)
66. Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Remsen J, O'Grady P, Mol Phylogenet Evol 2002 24 2 249 264 10.1016/S1055-7903(02)00226-9 12144760 (Pubitemid 34995917)
67. Phylogenetic studies of ribosomal RNA variation in higher moths and butterflies (Lepidoptera: Ditrysia). Weller SJ, Friedlander TP, Martin JA, Pashley DP, Mol Phylogenet Evol 1992 1 4 312 337 10.1016/1055-7903(92)90007-4 1342947
68. Re: Phylogenetic relationships in Sphingidae (Insecta: Lepidoptera): initial evidence from two nuclear genes. Regier JC, Mitter C, Friedlander TP, Peigler RS, Mol Phylogenet Evol 2001 20 2 311 316 10.1006/mpev.2001.0963 11476639 (Pubitemid 32739557)
69. Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T, Mol Biol Evol 2003 20 6 907 913 10.1093/molbev/msg097 12716997 (Pubitemid 36578717)
70. Phylogeny of insect orders. Kristensen NP, Annu Rev Entomol 1981 26 135 157 10.1146/annurev.en.26.010181.001031
71. The streptisera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC, Syst Biol 1997 46 1 68 11975347 (Pubitemid 127365607)
72. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, Winterton SL, Yeates DK, BMC Biol 2009 7 34 10.1186/1741-7007-7-34 19552814
73. R Development Core Team, R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing 2009
74. Bayes empirical bayes inference of amino acid sites under positive selection. Yang Z, Wong WS, Nielsen R, Mol Biol Evol 2005 22 4 1107 1118 10.1093/molbev/msi097 15689528 (Pubitemid 40471423)