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Independent Elaboration of Steroid Hormone Signaling Pathways in Metazoans

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Independent Elaboration of Steroid Hormone Signaling Pathways in Metazoans Independent elaboration of steroid hormone signaling pathways in metazoans Gabriel V. Markova,b, Raquel Tavaresc,d, Chantal Dauphin-Villemante, Barbara A. Demeneixb, Michael E. Bakerf, and Vincent Laudeta,1 aMolecular Zoology Team, Institut de Ge´nomique Fonctionnelle de Lyon, Universite´de Lyon, Universite´Lyon 1 and Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Ecole Normale Supe´rieure de Lyon, 46 alle´e d’Italie, 69364 Lyon Cedex 07, France; bUnite´Mixte de Recherche 7221, Evolution des Re´gulations Endocriniennes, Muse´um National d’Histoire Naturelle, 75005 Paris, France; cUniversite´de Lyon, Universite´ Lyon 1, F-69000 Lyon, France; dCentre National de la Recherche Scientifique, Unite´Mixte de Recherche 5558, Laboratoire de Biome´trie et Biologie Evolutive, F-69622 Villeurbanne, France; eUnite´Mixte de Recherche 7622, Biologie du Developpement, Equipe Biogene`se des Signaux Hormonaux, Centre National de la Recherche Scientifique, Universite´Paris 6, 75005 Paris, France; and fDepartment of Medicine, University of California at San Diego, La Jolla, CA 92093-0693 Edited by Jan-A˚ ke Gustafsson, Karolinska Institutet, Stockholm, Sweden, and approved May 26, 2009 (received for review December 4, 2008) Steroid hormones regulate many physiological processes in verte- ple, it implies that 17ß-estradiol (E2) was a ligand for an ER in brates, nematodes, and arthropods through binding to nuclear re- Urbilateria, the common ancestor of protostomes and deuteros- ceptors (NR), a metazoan-specific family of ligand-activated transcrip- tomes (10, 12, 13). Such a hypothesis can be tested by searching for tion factors. The main steps controlling the diversification of this the origins of the enzymes involved in the synthesis of vertebrate family are now well-understood. In contrast, the origin and evolution adrenal and sex steroids. of steroid ligands remain mysterious, although this is crucial for As to steroid hormones in metazoans, there are major structural understanding the emergence of modern endocrine systems. Using a differences among different classes of steroids synthesized in ver- comparative genomic approach, we analyzed complete metazoan tebrates, insects and nematodes (Fig. S1). In insects and nematodes, genomes to provide a comprehensive view of the evolution of major the active steroid hormones retain all or most of the C17 side chain enzymatic players implicated in steroidogenesis at the whole meta- of cholesterol, with selective hydroxylations providing specificity for zoan scale. Our analysis reveals that steroidogenesis has been inde- a given NR (Fig. 1C) (14–16). In contrast, in vertebrates, such as pendently elaborated in the 3 main bilaterian lineages, and that humans, synthesis of the main active steroids [estradiol for ERs, steroidogenic cytochrome P450 enzymes descended from those that dihydroxytestosterone (DHT) for AR, progesterone (P4) for PR, detoxify xenobiotics. cortisol for GR, and aldosterone for MR] begins with cleavage of the C17 side chain at C20 by CYP11A1 to yield pregnenolone (P5) evolution ͉ nuclear-receptor ligand ͉ steroidogenesis (Fig. 1B) (17). Further enzymatic modifications involving selective hydroxylations, oxido-reductions and isomerizations of P5 and ulticellular organisms have complex endocrine systems, al- its metabolites yield ligands for adrenal and sex steroid receptors Mlowing responses to environmental stimuli, regulation of (Fig. 1B). development, reproduction, and homeostasis. Nuclear receptors Many searches for ‘‘human’’-type steroid hormones such as E2 or (NRs), a metazoan-specific family of ligand-activated transcription P4, throughout metazoan groups have been prone to artefacts factors, play central roles in endocrine responses, as intermediates and/or misidentification. To date, biochemical evidence (immuno- between signaling molecules and target genes (1). The NR family logical and/or chromatographic methods linked to mass spectrom- includes ligand-bound and orphan receptors, that is, receptors with etry) for presence of vertebrate steroids in lophotrochozoans, no known ligand or for which there is no ligand pocket (2). ecdysozoans, and cnidarians have not been substantiated by mo- Understanding NR evolution has been further improved by com- lecular characterization of enzymes directly involved in their de parison of several completed genomes, particularly those of deu- novo biosynthesis (18, 19). Thus, the presence of human-type BIOCHEMISTRY terostomes and ecdysozoans (3–6). steroids in protostomes remains an open question. In contrast, evolution of NR ligands is still much debated. One With this in mind, we investigated origins of enzymes in the hypothesis proposes that several independent gains and losses of pathways leading to steroid hormones in vertebrates. Our phylo- ligand-binding ability in NRs occurred in protostomes and deuter- genetic analyses of all enzymes known to be implicated in vertebrate ostomes (7–9). A second hypothesis, pertaining to the NR3 sub- (Fig. 1B) or ecdysozoan (Fig. 1C) steroid biosynthesis [belonging to family (vertebrate steroid hormone receptors and estrogen-related the cytochrome P450 (CYP, 20, 21), short-chain dehydrogenase/ reductase (SDR, 22), 3-ß hydroxysteroid dehydrogenase (HSD3B, receptor), proposes that before the divergence of protostomes and ␣ deuterostomes, there was an ancestral steroid receptor (AncSR) 23) and steroid 5- reductase (SRD5A) families] suggest that that was ligand-activated and that orphan receptors secondarily lost steroidogenesis was independently elaborated in vertebrates and the ability to bind a ligand (10, 11). Phylogenetic analyses indicate protostomes, partly through recruitment of xenobiotic-metabolis- ing CYPs. This has important implications on our views about the that AncSR was able to bind estrogens (10, 11), which formed the basis for an intriguing ‘‘ligand exploitation model’’ (10, 12) for the evolution of vertebrate steroid receptors. In this model, estradiol Author contributions: G.V.M. and V.L. designed research; G.V.M. performed research; (E2), a terminal product of the steroid biosynthetic pathway, was G.V.M., R.T., and V.L. analyzed data; and G.V.M., C.D.-V., B.A.D., M.E.B., and V.L. wrote the the first ligand for AncSR. Synthesis of E2 also requires the paper. synthesis of steroid intermediates (Fig. 1). However, receptors for The authors declare no conflict of interest. these intermediate steroids had not yet evolved. It was only after This article is a PNAS Direct Submission. duplication of AncSR that NR3 receptors for these intermediate 1To whom correspondence should be addressed at: Universite´de Lyon, Universite´Lyon 1, steroids evolved. The ‘‘ligand exploitation model’’ explains diver- Ecole Normale Supe´rieure de Lyon, Institut de Ge´nomique Fonctionnelle de Lyon, Equipe gence in ligand specificity seen in steroid receptors, namely AR/ de Zoologie Mole´culaire, Centre National de la Recherche Scientifique, Unite´Mixte de Recherche 5242, Institut National de la Recherche Agronomique, Unite´Mixte de Recher- NR3C4, GR/NR3C1, MR/NR3C2, PR/NR3C3, and ERs/NR3A che 1237, 46 Alle´e d’Italie, 69364 Lyon Cedex 07, France. E-mail: vincent.laudet@ (10, 12, Fig. 1A and B). ens-lyon.fr. The ligand exploitation model is based mainly on NR data. But This article contains supporting information online at www.pnas.org/cgi/content/full/ it has implications for the evolution of ligand synthesis. For exam- 0812138106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0812138106 PNAS ͉ July 21, 2009 ͉ vol. 106 ͉ no. 29 ͉ 11913–11918 Downloaded by guest on September 29, 2021 for phylogenetic reconstruction (using maximum likelihood cou- pled with bootstrapping) to determine their orthology with verte- brate sequences. Orthology was defined on the basis of robust branches containing a consistent phylogenetic sampling (that is only protostome se- quences for example) and/or high (Ͼ90%) bootstrap values. The large sequence variability present in some families such as CYPs precluded phylogenetic reconstruction, but our systematic survey revealed clear orthology in specific cases relevant to steroidogenesis evolution (24, 25). Twenty-one complete genomes were screened, including 6 re- cently sequenced lophotrochozoan genomes, making it highly prob- able that not finding a given protein in a given zoological group (e.g., protostomes) indicates a real absence. Fig. 1A exemplifies our reasoning for estrogen receptors. Our strategy successfully identified clear orthologs of known steroidogenic enzymes. For example, we identified in Daphnia,a crustacean, orthologs of enzymes that metabolize insect steroids (i.e., CYP302, CYP314, CYP315, and CYP306) known in Drosoph- ila and other insects (Fig. 2A and Fig. 3 and Figs. S3 and S4). Fig. 2 provides a general overview of the phylogeny of the 4 protein families analyzed. For more complete versions of these phylogenies, and the relevant specific branches see Figs. S3–S7. These phylogenies, based on several sequenced genomes, are in good agreement with published studies (25). Polyphyletic Origin for Steroidogenic CYPs. The metazoan CYP family is currently divided into 11 clans (21, 22, Fig. 2A and Fig. S3), including the mito clan that clusters mitochondrial proteins in vertebrates and insects (Fig. 3 and Fig. S4). To date, all mitochon- drial CYPs identified in vertebrates are involved in metabolism of endogenous compounds (e.g., CYP27A1 for bile acids) or hormone biosynthesis (CYP11A and CYP11B for steroid hormones), with
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