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Research/0018.1 http://genomebiology.com/2001/2/6/research/0018.1 Research The human olfactory receptor repertoire comment Sergey Zozulya, ernando Echeverri and Trieu Nguyen Address: Senomyx Inc., 11099 North Torrey Pines Road, La Jolla, CA 92037, USA. Correspondence: Sergey Zozulya. E-mail: [email protected] reviews Published: 1 June 2001 Received: 8 March 2001 Revised: 12 April 2001 Genome Biology 2001, 2(6):research0018.1–0018.12 Accepted: 18 April 2001 The electronic version of this article is the complete one and can be found online at http://genomebiology.com/2001/2/6/research/0018 © 2001 Zozulya et al., licensee BioMed Central Ltd (Print ISSN 1465-6906; Online ISSN 1465-6914) reports Abstract Background: The mammalian olfactory apparatus is able to recognize and distinguish thousands of structurally diverse volatile chemicals. This chemosensory function is mediated by a very large family of seven-transmembrane olfactory (odorant) receptors encoded by approximately 1,000 genes, the majority of which are believed to be pseudogenes in humans. deposited research Results: The strategy of our sequence database mining for full-length, functional candidate odorant receptor genes was based on the high overall sequence similarity and presence of a number of conserved sequence motifs in all known mammalian odorant receptors as well as the absence of introns in their coding sequences. We report here the identification and physical cloning of 347 putative human full-length odorant receptor genes. Comparative sequence analysis of the predicted gene products allowed us to identify and define a number of consensus sequence motifs and structural features of this vast family of receptors. A new nomenclature for human odorant receptors based on their chromosomal localization and phylogenetic analysis is proposed. refereed research We believe that these sequences represent the essentially complete repertoire of functional human odorant receptors. Conclusions: The identification and cloning of all functional human odorant receptor genes is an important initial step in understanding receptor-ligand specificity and combinatorial encoding of odorant stimuli in human olfaction. interactions Background a sophisticated mechanism of OR gene choice. Another Olfaction is a major neurosensory function by which intriguing feature of olfaction is combinatorial recognition of mammals investigate the external chemical environment. odorants. Each receptor recognizes multiple odorants, and The initial step in odor identification is interaction of an each odorant binds to multiple receptors to generate specific odorant molecule with olfactory (odorant) receptors (ORs) activation patterns for each of a vast number of distinct expressed at the surface of cilia of chemosensory olfactory smells [10]. neurons in the olfactory epithelium. Seven-transmembrane information ORs, first identified in 1991 [1], are the largest vertebrate The genes encoding ORs are devoid of introns within their gene family, comprising as many as 1,000 genes (reviewed in coding regions [1,11]. Mammalian OR genes are typically [2-6]). Mammalian ORs are classical G-protein-coupled organized in clusters of ten or more members and located on receptors belonging to Class I or A, which also includes many chromosomes [12-14]. The repertoire of human OR opsins and catecholamine receptors [7]. Each olfactory (hOR) genes contains a large fraction of pseudogenes, sug- neuron appears to express a single type of OR [8-10] implying gesting that olfaction became less important in the course of 2 Genome Biology Vol 2 No 6 Zozulya et al. primate evolution. Recent studies indicate that some 70% of all hOR genes may be pseudogenes, compared with fewer NCBI resources: than 5% in rodents or lower primates [15,16]. Medline, LocusLink, Entrez, OMIM Analyses of incomplete compilations of hORs, in particular HORDE database at Weizmann Institute approximately 150 full-length receptor genes [17,18], have Olfactory Receptor Database (ORDB) at recently been published. A larger annotated set of hOR genes Yale University is available as an online database [19]. The very recent mile- stone publication of the first draft of the human genome sequence by two groups [20,21] opens up the possibility of Keyword search detailed and complete identification, mapping and analysis of OR genes and their products in the near future. One of Initial hOR query set these groups reported that the human genome contains 906 OR genes, of which approximately 60% appear to be pseudo- 1. TBLASTN, BLASTN, BLASTP searches genes [20]. Many alternative nomenclatures for hORs, of NCBINR, HTGS, hEST, GSS, STS including a comprehensive phylogenetic classification devel- Refine query set sequence databases oped at the Weizmann Institute [17,22], have been proposed 2. ORF Finder, alignment with known by various labs over the past few years. ORs signature motif analysis The identification, cloning and sequence-based classification Putative full-length hOR sequence set and analysis of candidate hORs are essential prerequisites for rational structure-function studies of this vast receptor Validation: family. Our goal was to identify the complete repertoire of cloning by genomic PCR, hOR genes encoding full-length receptors. The approach was sequencing to carry out reiterative homology-based searches of Database of human functional GenBank DNA, particularly recently available unannotated olfactory receptor candidates raw sequences, and to compile hOR sequences already present in other public databases. We report here the identi- fication and cloning of 347 putative full-length hOR receptor Figure 1 genes, which we believe accounts for nearly the entire reper- Flow diagram for OR gene discovery by database mining. toire of functional hORs. We also present a comparative sequence analysis of the predicted OR gene products and propose a new nomenclature for candidate hORs. below) hOR genes and a large number of candidate sequence fragments. Results and discussion The next step was identification of additional members of Sequence database mining and odorant receptor the family by exhaustive iterative homology searches of cloning translated human genomic sequence databases, particularly The general strategy for the search for full-length hOR genes the raw, unannotated high-throughput genomic sequences is shown in igure 1. It was based on absence of introns in (HTGS), using protein queries corresponding to the known coding sequences of mammalian ORs [1,11] as well as high hORs. As the number of identified receptors grew, additional overall sequence similarity and the presence of several diverse sequences were added to the query list to capture highly conserved sequence motifs in all known mammalian additional ORs in databases. Genomic sequences containing ORs [2]. areas of significant homology to ORs were subjected to open reading frame (OR) searches. Several hundred identified The first step was to identify all currently known hOR ORs of sufficient length (>250 amino acids) were trans- sequences by extensive keyword and homology-based lated and compared to known ORs. Three criteria were used searches of several public DNA and protein sequence data- to select putative ORs from this set: high overall sequence bases (see Materials and methods). The resulting several similarity, the presence of seven predicted transmembrane hundred sequences were compared with each other by (TM) regions, and the presence of multiple positionally con- BLAST and multiple sequence alignments. DNA and protein served sequence motifs, described in Materials and methods, entries were matched. All duplicates were cross-referenced that serve as signatures of this gene family. The basic criteria and apparent pseudogenes having frameshifts, deletions and for recognizing a particular OR gene as encoding a full- other defects obviously incompatible with receptor function length, functional receptor candidate were the presence of were eliminated. This initial screen identified approximately an uninterrupted OR starting with an ATG codon and a 90 bona fide full-length (according to criteria described complete seven-transmembrane unit. A few putative ORs http://genomebiology.com/2001/2/6/research/0018.3 were discarded from the final set because they contained shown in the multiple sequence alignment (igure 2) are structural features deemed to be incompatible with receptor those extracted from genomic sequence database entries. function, such as insertions of multiple nucleotide sequence comment repeats in their ORs. Studies of human OR gene and pseudogene sequences cover- ing approximately 150 full-length receptor genes [17,18] These are intentionally minimalist criteria designed to were recently published. A larger set of annotated putative exclude apparent OR pseudogenes, but not cryptic pseudo- human OR genes identified by an automated search algo- genes, such as those having defects on the level of transcrip- rithm became very recently accessible through a worldwide tion or splicing or containing subtle but functionally web interface [19]. A detailed comparison and cross-refer- disruptive mutations in receptor coding region. or example, encing of this overlapping set of data with the output of our human OR17-24 (hOR17.01.01 in our nomenclature as dis- independent database mining and genomic cloning effort reviews cussed below) classified by others [23] as a probable pseudo- allowed us to verify the hOR selection reported in this paper. gene on the basis of deviations from other ORs in its The
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