Structural and evolutionary innovation of the heterodimerization interface between USP and the ecdysone receptor ECR in insects

Molecular Biology and Evolution

Volumn 26, Issue 4, 2009, Pages 753-768

  Iwema, Thomas ^a,b,c,d,i   Chaumot, Arnaud ^e   Studer, Romain A ^f,g   Robinson Rechavi, Marc ^f,g   Billas, Isabelle M L ^a,b,c,d   Moras, Dino ^a,b,c,d   Laudet, Vincent ^h   Bonneton, François ^h  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e CEMAGREF   (France)

^f UNIVERSITY OF LAUSANNE   (Switzerland)

^g SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^h UNIVERSITÉ DE LYON   (France)

ⁱ INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

3D structure; Epistasis; Heterodimerization; Mecopterida; Nuclear receptors

Indexed keywords

ANIMALS; INSECT PROTEINS; INSECTS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, STEROID; STRUCTURAL HOMOLOGY, PROTEIN;

ARTHROPODA; HELIOTHIS; HEXAPODA; LEPIDOPTERA; VERTEBRATA;

EID: 62349134544     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn302     Document Type: Article

References (66)

1. Benoit G, Malewicz M, Perlmann T. 2004. Digging deep into the pockets of orphan nuclear receptors: insights from structural studies. Trends Cell Biol. 14:369-376.
2. Bergman T, Henrich V, Schlattner U, Lezzi M. 2004. Ligand control of interaction in vivo between ecdysteroid receptor and ultraspiracle ligand-binding domain. Biochem J. 378:779-784.
3. Bertrand S, Brunet F, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M. 2004. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol Biol Evol. 21:1923-1937.
4. Billas I, Iwema T, Garnier J, Mitschler A, Rochel N, Moras D. 2003. Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature. 426:91-96.
5. Billas I, Moras D. 2005. Ligand-binding pocket of the ecdysone receptor. Vitam Horm. 73:101-129.
6. Billas I, Moulinier L, Rochel N, Moras D. 2001. Crystal structure of the ligand-binding domain of the ultraspiracle protein USP, the ortholog of retinoid X receptors in insects. J Biol Chem. 276:7465-7474.
7. Bonneton F, Brunet F, Kathirithamby J, Laudet V. 2006. The rapid divergence of the ecdysone receptor is a synapomorphy for Mecopterida that clarifies the Strepsiptera problem. Insect Mol Biol. 15:351-362.
8. Bonneton F, Chaumot A, Laudet V. 2008. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochem Mol Biol. 38:416-429.
9. Bonneton F, Zelus D, Iwema T, Robinson-Rechavi M, Laudet V. 2003. Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR. Mol Biol Evol. 20:541-553.
10. Bourguet W, Vivat V, Wurtz J, Chambon P, Gronemeyer H, Moras D. 2000. Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol Cell. 5:289-298.
11. Carmichael J, Lawrence M, Graham L, et al. (11 co-authors). 2005. 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. J Biol Chem. 280:22258-22269.
12. Clayton G, Peak-Chew S, Evans R, Schwabe J. 2001. The structure of the ultraspiracle ligand-binding domain reveals a nuclear receptor locked in an inactive conformation. Proc Natl Acad Sci USA. 98:1549-1554.
13. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 50:760-763.
14. Dutheil J, Pupko T, Jean-Marie A, Galtier N. 2005. A model-based approach for detecting coevolving positions in a molecule. Mol Biol Evol. 22:1919-1928.
15. Folkertsma S, van Noort P, Brandt R, Bettler E, Vriend G, de Vlieg J. 2005. The nuclear receptor ligand-binding domain: a family-based structure analysis. Curr Med Chem. 12:1001-1016.
16. Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 12: 543-548.
17. Gampe RJ, Montana V, Lambert M, Miller A, Bledsoe R, Milburn M, Kliewer S, Willson T, Xu H. 2000. Asymmetry in the PPARgamma/RXRalpha crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol Cell. 5:545-555.
18. García-Serna R, Opatowski L, Mestres J. 2006. FCP: functional coverage of the proteome by structures. Bioinformatics. 22:1792-1793.
19. Giribet G, Edgecombe G, Wheeler W. 2001. Arthropod phylogeny based on eight molecular loci and morphology. Nature. 413:157-161.
20. Graham L, Pilling P, Eaton R, et al. (10 co-authors). 2007. Purification and characterization of recombinant ligand-binding domains from the ecdysone receptors of four pest insects. Protein Expr Purif. 53:309-324.
21. Grantham R. 1974. Amino acid difference formula to help explain protein evolution. Science. 185:862-864.
22. Guex N, Peitsch M. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:2714-2723.
23. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
24. Hayward D, Dhadialla T, Zhou S, Kuiper M, Ball E, Wyatt G, Walker V. 2003. Ligand specificity and developmental expression of RXR and ecdysone receptor in the migratory locust. J Insect Physiol. 49:1135-1144.
25. Henrich V. 2005. The ecdysteroid receptor. Comprehensive molecular insect science. Elsevier.
26. Hwang U, Friedrich M, Tautz D, Park C, Kim W. 2001. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature. 413:154-157.
27. IJpenberg A, Tan N, Gelman L, et al. 10 co-authors). 2004. In vivo activation of PPAR target genes by RXR homodimers. EMBO J. 23:2083-2091.
28. Iwema T, Billas I, Beck Y, Bonneton F, Nierengarten H, Chaumot A, Richards G, Laudet V, Moras D. 2007. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. EMBO J. 26:3770-3782.
29. Jones D, Taylor W, Thornton J. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
30. Khorasanizadeh S, Rastinejad F. 2001. Nuclear-receptor interactions on DNA-response elements. Trends Biochem Sci. 26:384-390.
31. Knudsen B, Miyamoto M. 2001. A likelihood ratio test for evolutionary rate shifts and functional divergence among proteins. Proc Natl Acad Sci USA. 98:14512-14517.
32. Koelle M, Talbot W, Segraves W, Bender M, Cherbas P, Hogness D. 1991. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 67:59-77.
33. Kristensen NP. 1981. Phylogeny of insect orders. Annu Rev Entomol. 135-157.
34. Laskowski R, Thornton J. 2008. Understanding the molecular machinery of genetics through 3D structures. Nat Rev Genet. 9:141-151.
35. Laudet V, Gronemeyer H. 2002. The nuclear receptor facts book. London: Academic Press.
36. Lee B, Richards F. 1971. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 55:379-400.
37. Lezzi M, Bergman T, Henrich V, Vögtli M, Frömel C, Grebe M, Przibilla S, Spindler-Barth M. 2002. Ligand-induced heterodimerization between the ligand binding domains of the Drosophila ecdysteroid receptor and ultraspiracle. Eur J Biochem. 269:3237-3245.
38. Li C, Schwabe J, Banayo E, Evans R. 1997. Coexpression of nuclear receptor partners increases their solubility and biological activities. Proc Natl Acad Sci USA. 94: 2278-2283.
39. Li Y, Lambert M, Xu H. 2003. Activation of nuclear receptors: a perspective from structural genomics. Structure. 11:741-746.
40. Mader S, Chen J, Chen Z, White J, Chambon P, Gronemeyer H. 1993. The patterns of binding of RAR, RXR and TR homo- and heterodimers to direct repeats are dictated by the binding specificites of the DNA binding domains. EMBO J. 12:5029-5041.
41. Maestro O, Cruz J, Pascual N, Martín D, Bellés X. 2005. Differential expression of two RXR/ultraspiracle isoforms during the life cycle of the hemimetabolous insect Blattella germanica (Dictyoptera, Blattellidae). Mol Cell Endocrinol. 238:27-37.
42. Melo F, Feytmans E. 1998. Assessing protein structures with a non-local atomic interaction energy. J Mol Biol. 277: 1141-1152.
43. Minakuchi C, Ogura T, Miyagawa H, Nakagawa Y. 2007. Effects of the structures of ecdysone receptor (EcR) and ultraspiracle (USP) on the ligand-binding activity of the EcR/USP heterodimer. J Pestic Science. 32:379-384.
44. Nakagawa Y, Sakai A, Magata F, Ogura T, Miyashita M, Miyagawa H. 2007. Molecular cloning of the ecdysone receptor and the retinoid X receptor from the scorpion Liocheles australasiae. FEBS J. 274:6191-6203.
45. Nowickyj S, Chithalen J, Cameron D, Tyshenko M, Petkovich M, Wyatt G, Jones G, Walker V. 2008. Locust retinoid X receptors: 9-Cis-retinoic acid in embryos from a primitive insect. Proc Natl Acad Sci USA. 105:9540-9545.
46. Ogura T, Minakuchi C, Nakagawa Y, Smagghe G, Miyagawa H. 2005. Molecular cloning, expression analysis and functional confirmation of ecdysone receptor and ultraspiracle from the Colorado potato beetle Leptinotarsa decemlineata. FEBS J. 272:4114-4128.
47. Regier J, Mitter C, Friedlander T, Peigler R. 2001. Re: phylogenetic relationships in Sphingidae (Insecta: lepidoptera): initial evidence from two nuclear genes. Mol Phylogenet Evol. 20:311-316.
48. Robinson-Rechavi M, Maina C, Gissendanner C, Laudet V, Sluder A. 2005. Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. J Mol Evol. 60:577-586.
49. Savard J, Tautz D, Lercher M. 2006. Genome-wide acceleration of protein evolution in flies (Diptera). BMC Evol Biol. 6:7.
50. Savard J, Tautz D, Richards S, Weinstock G, Gibbs R, Werren J, Tettelin H, Lercher M. 2006. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res. 16:1334-1338.
51. Schulman I, Heyman R. 2004. The flip side: identifying small molecule regulators of nuclear receptors. Chem Biol. 11:639-646.
52. Schwede T, Kopp J, Guex N, Peitsch M. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
53. Suino K, Peng L, Reynolds R, Li Y, Cha J, Repa J, Kliewer S, Xu H. 2004. The nuclear xenobiotic receptor CAR: structural determinants of constitutive activation and heterodimerization. Mol Cell. 16:893-905.
54. Thomas H, Stunnenberg H, Stewart A. 1993. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature. 362:471-475.
55. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger P, Mark AE, Scott WRP, Tironi IG. 1996. Biomolecular simulation: the GROMOS96 manual and user guide. Vdf Hochschulverlag ETHZ. Zürich (Grogingen): Zürich 2nd BIOMOS b.v.
56. Vivat-Hannah V, Bourguet W, Gottardis M, Gronemeyer H. 2003. Separation of retinoid X receptor homo- and heterodimerization functions. Mol Cell Biol. 23:7678-7688.
57. Weller S, Friedlander T, Martin J, Pashley D. 1992. Phylogenetic studies of ribosomal RNA variation in higher moths and butterflies (Lepidoptera: Ditrysia). Mol Phylogenet Evol. 1:312-337.
58. Whiting M, Carpenter J, Wheeler Q, Wheeler W. 1997. The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol. 46:1-68.
59. Xu R, Lambert M, Wisely B, et al. (11 co-authors). 2004. A structural basis for constitutive activity in the human CAR/ RXR alpha heterodimer. Mol Cell. 16:919-928.
60. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
61. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics. 141:1641-1650.
62. Yang Z, Wang T. 1995. Mixed model analysis of DNA sequence evolution. Biometrics. 51:552-561.
63. Yao T, Forman B, Jiang Z, Cherbas L, Chen J, McKeown M, Cherbas P, Evans R. 1993. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature. 366:476-479.
64. Yao T, Segraves W, Oro A, McKeown M, Evans R. 1992. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell. 71:63-72.
65. Yeates D, Wiegmann B. 1999. Congruence and controversy: toward a higher-level phylogeny of Diptera. Annu Rev Entomol. 44:397-428.
66. Zdobnov E, Bork P. 2007. Quantification of insect genome divergence. Trends Genet. 23:16-20.