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BMC Genomics Biomed Central BMC Genomics BioMed Central Research article Open Access The repertoire of G-protein-coupled receptors in Xenopus tropicalis Yanping Ji, Zhen Zhang and Yinghe Hu* Address: Shanghai Institute of Brain Functional Genomics, East China Normal University, 3663 Zhongshan Road N., Shanghai, 200062, PR China Email: Yanping Ji - [email protected]; Zhen Zhang - [email protected]; Yinghe Hu* - [email protected] * Corresponding author Published: 9 June 2009 Received: 25 November 2008 Accepted: 9 June 2009 BMC Genomics 2009, 10:263 doi:10.1186/1471-2164-10-263 This article is available from: http://www.biomedcentral.com/1471-2164/10/263 © 2009 Ji et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The G-protein-coupled receptor (GPCR) superfamily represents the largest protein family in the human genome. These proteins have a variety of physiological functions that give them well recognized roles in clinical medicine. In Xenopus tropicalis, a widely used animal model for physiology research, the repertoire of GPCRs may help link the GPCR evolutionary history in vertebrates from teleost fish to mammals. Results: We have identified 1452 GPCRs in the X. tropicalis genome. Phylogenetic analyses classified these receptors into the following seven families: Glutamate, Rhodopsin, Adhesion, Frizzled, Secretin, Taste 2 and Vomeronasal 1. Nearly 70% of X. tropicalis GPCRs are represented by the following three types of receptors thought to receive chemosensory information from the outside world: olfactory, vomeronasal 1 and vomeronasal 2 receptors. Conclusion: X. tropicalis shares a more similar repertoire of GPCRs with mammals than it does with fish. An examination of the three major groups of receptors related to olfactory/pheromone detection shows that in X. tropicalis, these groups have undergone lineage specific expansion. A comparison of GPCRs in X. tropicalis, teleost fish and mammals reveals the GPCR evolutionary history in vertebrates. Background roidism, nephrogenic diabetes insipidus, several fertility The G-protein-coupled receptor (GPCR) superfamily rep- disorders and carcinomas [3]. GPCRs are the richest resents the largest protein family in the human genome source of targets for the pharmaceutical industry [4]. [1,2]. These proteins have ancient origins and their sequences are very diverse in a number of species. None- The evolutionary data for GPCRs can be applied to further theless, all GPCRs share a common molecular architecture functional analyses and are particularly useful for struc- consisting of seven transmembrane (TM) domains. tural evaluation of disease-causing mutations. In this GPCRs transduce outside signals to intracellular effectors respect, because of their common physiological traits with and play a central role in almost all physiological func- all vertebrates, amphibians can be ideal non-mammalian tions. The disruption of their normal activities in humans models for GPCR-related functional and medical research results in a wide variety of diseases and disorders, includ- [5]. Although the overall repertoires of GPCRs have been ing retinitis pigmentosa (RP), hypo- and hyperthy- documented in teleost fish [6] and mammals [7,8], no Page 1 of 12 (page number not for citation purposes) BMC Genomics 2009, 10:263 http://www.biomedcentral.com/1471-2164/10/263 such report yet exists for amphibians. However, recent Phylogenetic analysis was performed for strict family clas- developments relating to genomic sequence data have sification. With regard to the large number of genes for allowed us to conduct extensive analyses of the amphib- olfactory receptors and CaSR like receptors (consisting of ian GPCR family, which may help us to understand the extracellular calcium-sensing receptors and pheromone connections in the GPCR evolution from teleost fish to receptors) would hamper the preliminary phylogenetic mammals. analysis, the positions of the two groups were established by diverse receptors of the two groups using CD-HIT 40% For this purpose, we chose the western clawed frog Xeno- sequence identity. The phylogenetic analysis first sepa- pus (Silurana) tropicalis for our investigation. X. tropicalis is rated the GPCR sequences into rhodopsin like receptors a preferred model for genetic studies because it has a and non-rhodopsin like receptors, then separated the rho- smaller diploid genome than that of its relatives. Recently, dopsin like receptors into six families. In addition to the its genome has been sequenced, and the sequences have five main GPCR families (GRAFS: Glutamate (G), Rho- been released in the form of scaffolds. In this study, we dopsin (R), Adhesion (A), Frizzled (F) and Secretin (S) present a strategy for detecting and identifying GPCR [8]), Taste 2 receptors (T2Rs) and Vomeronasal 1 recep- genes from a genomic assembly. Using this strategy, we tors (V1Rs) were considered as two independent receptor have provided the first overall map of the GPCRs in X. families (Figure 2). Besides the above seven families, nine tropicalis. By comparing X. tropicalis receptor groups with other X. tropicalis GPCRs that could not be classified into those of mammals and/or fish, we performed detailed any of these families were referred to as "Other GPCRs". phylogenetic analyses. These comparative data provide Figure 3 compares the distribution of a number of differ- information about the evolutionary history of GPCRs, ent GPCR families in X. tropicalis with those from six dif- and the available receptor sequences may help to identify ferent species [6,7,11-13]. The main difference in the conserved sequence motifs that are responsible for certain GPCR repertoire between X. tropicalis and other species aspects of GPCR functionality, especially those which may genomes is the number of vomeronasal 2 receptors cause disease through mutation. (V2Rs) in Glutamate receptor family. Results and Discussion The Adhesion (24 members), Frizzled (11 members) and The overall GPCR repertoire in Xenopus tropicalis Secretin (16 members) families The genome of X. tropicalis is estimated to be approxi- In the phylogenetic tree (Figure 4A), 24 Adhesion receptors mately 1.7 billion base pairs contained in 10 pairs of chro- of X. tropicalis were compared with the related receptors in mosomes. The protein sequences used in our research humans. The I-VIII groups of the Adhesion family based on were obtained from the Joint Genome Institute's X. tropi- phylogeny [14] are shown in the tree. There are 17 cases calis genome project [9]. The current database, JGI Xenopus of one-to-one orthologous relationships between human tropicalis v4.1, contains 27,917 protein sequences. As the and X. tropicalis Adhesion receptors, while the ortholog to protein sequences represent approximately 95% of the human EGF-TM7-latrophilin-related protein (ETL) recep- full-length cDNAs of X. tropicalis, we expect that the GPCR tor and EGF-like modules containing mucin-like receptor genes identified here comprise the majority of the GPCR proteins (EMRs) seem to be missing in X. tropicalis. The repertoire in X. tropicalis. The gene sequences of X. tropica- location of brain-specific angiogenesis-inhibitory receptor lis have been released in the form of scaffolds, so highly 1 (BAI1) in X. tropicalis could not be calculated in this tree, polymorphic genes might be overestimated. In order to but its one-to-one human ortholog was determined avoid overestimation, CD-HIT [10] 90% sequence iden- (Additional file 3). tity was applied to remove polymorphisms, splice vari- ants, pseudogenes and duplicates from the database. One smoothened receptor and 10 frizzled receptors were identified in X. tropicalis, which was in agreement with the Using the strategy shown in Figure 1, 1,452 GPCRs were findings in both humans [8] and chickens [11]. Figure 4B identified. GPCRs represent about 5.2% of the total describes the relationship between human and X. tropicalis number of genes predicted from the X. tropicalis genome. Frizzled receptors. Indeed, it can be seen that this family Homologues of the chemosensory GPCRs from nema- displays 100% ortholog conservation between humans todes, plant GPCRs, yeast pheromone receptors, or insect and X. tropicalis. This high conservation could be related gustatory and olfactory receptors were not identified. The to their crucial role in early embryonic development [15]. X. tropicalis receptors were named after their closest known GPCRs by BLASTP against the NCBI non-redun- The X. tropicalis genome contains 16 Secretin receptors, dant database. The names in each family are listed in while the human genome contains 15. There is a high Additional file 1 and the sequences of each receptor are degree of 13 one-to-one orthologs between humans and listed in Additional file 2. X. tropicalis (Figure 4C). Only the calcitonin receptor Page 2 of 12 (page number not for citation purposes) BMC Genomics 2009, 10:263 http://www.biomedcentral.com/1471-2164/10/263 SequenceFigure 1 analysis strategy for the identification of X. tropicalis GPCRs Sequence analysis strategy for the identification of X. tropicalis GPCRs. Two parallel methods were used for search- ing the crude sequence database. One was retrieval of proteins with six to eight TM domains from the X. tropicalis proteome database, and the other was extraction of the BLASTP top 20 hits by comparing the GPCR sequences from GPCRDB against the X. tropicalis proteome database. The crude database, which eliminated polymorphism, splice variants, pseudogenes and duplicates by CD-HIT 90% sequence identity, was searched for GPCR conserved domains using CDD v2.14 (E-value = 10-4) and Plam 22.0 (E-value = 0.01). The sequences with conserved seven TM domain were searched using BLASTP against the NCBI non-redundant database. Phylogenetic analyses were carried out to separate the GPCR sequences into rhodopsin like receptors and non-rhodopsin like receptors. (CALCR) lacks a human ortholog. One of the two X.
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