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Analysis of the human genome draft sequences has revealed a more complete portrait of the olfactory receptor gene repertoire in humans than was available previously. The new information provides a basis for deeper analysis of the functions of the receptors, and promises new insights into the evolutionary history of the family.

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Olfactory receptors belong to the superfamily of G-protein-coupled receptors (GPCRs), which are characterized by seven transmembrane helical regions. For years it has been estimated that mammals have some 1,000 olfactory genes [8,9,10], making up the largest family in the genome. The family thus constitutes some 3% of the 31,000 genes now estimated to comprise the human genome. Before the complete draft genome sequence was available, Rouquier et al. [11] identified 72% of a sample of human olfactory receptor genes as pseudogenes (due to frame shifts and stop codons). A follow-up study [12] showed that loss of receptor function by the transformation of functional genes into pseudogenes is relatively common in human and prosimian primates, less common in lower primates, and is rarely found in mouse or zebrafish. The implication is that as species require less olfactory acuity, molecular disruptions accumulate and erode the functionality of olfactory receptor genes. The absence of functional olfactory receptors in the dolphin [13] and the deterioration of vision in moles [14] provide extreme examples of this mechanism, which is believed to account for the reduced olfactory acuity of humans compared to rodents and non-human primates.

Two recent publications [15,16] reporting data mining for olfactory receptors in the completed draft human genome have largely supported the earlier findings. Zozulya et al. [15] identified more than 347 full-length, functional olfactory receptor genes; Glusman et al. [16] reported 368 (see Figure 1). The number of pseudogenes identified in the two studies also compares well with the numbers of Rouquier et al. [11,12]. Glusman et al. [16] identified more than 900 olfactory receptor genes and pseudogenes, consistent with the earlier predictions [8,9,10]; of these, 681 are full-length, but only 322 are believed to be functional. They also detect some 70 full-length receptor genes that have yet to be assigned to any specific chromosome [16]. Detailed analysis of the human olfactory receptor family also enabled Glusman et al. [16] to infer diversification events in human evolution and a 'molecular clock' for the family, indicating the rate at which acquired mutations become fixed in the evolutionary lineage.

Using fluorescence in situ hybridization experiments, Rouquier et al. [12] determined that human olfactory receptor genes are distributed over all chromosomes except 20 and Y. Most of the receptor genes are present in two super-clusters on chromosome 11, which is taken to reflect the evolutionary origin of this family as a repeated cluster on a single chromosome [15,16]. Next in order of frequency are receptors on chromosomes 1, 9 and 6 and 14; chromosomes 10, 22 and X each carry only one olfactory receptor gene. In addition, none of the 347 genes encoding functional receptors that were identified by Zozulya et al. [15] was found on chromosomes 2, 4, 18 or 21.

Developing a systematic classification and nomenclature for this enormous gene family is a daunting task: sequence identity has been a starting point. The sequence identity between any two randomly selected olfactory receptor genes is generally 40% or higher. The lowest reported percentage identity for a pair approaches 20% [15]. Glusman et al. [16], who reported average protein sequence identities among olfactory receptors in agreement with those reported by Zozulya et al. [15], also calculated sequence relationships with 55 non-olfactory GPCR sequences. The average percentage identity of 27% for olfactory: non-olfactory pairs was lower than that for pairs of olfactory receptors.

It was initially suggested that olfactory receptor sequences with a percentage sequence identity of 40% or greater constitute a family, and sequences with sequence identity of 60% or greater a subfamily [17,18]. This convention has been applied by Glusman et al. [16] to the entire olfactory subgenome (see the Human Olfactory Receptor Data Exploratorium (HORDE) website [19]); for instance: the name hOR11H11 means that this receptor belongs to family 11 and is the eleventh gene of subfamily H. The classification scheme of Zozulya et al. [15] at Senomyx, Inc. (La Jolla, USA) is based on the chromosome number, the family number and a unique member identifier; an example of an olfactory receptor name thus identified would be hOR14.03.03, where the gene is identified as localized on chromosome 14, and is the third member of family 3. In this scheme, the sequence identity required for an olfactory receptor to qualify as a member of a family was 43%.

Earlier work identified olfactory receptor groupings characteristic of fish (Class 1) [21] and amphibians (Class 2) [22]. Glusman et al. [16] report that the genes for a large number of human olfactory receptors similar to Class I have fewer pseudogenes (52%) than those human olfactory receptors classified as similar to Class II (77%). On the basis of internal similarities between family members on different chromosomes, Glusman et al. [16] report evolutionary divergence and duplications depending on the subfamilies to which these receptor these genes belong.

Mining of the human genome and of other genomes soon to be revealed will give further insights into the functional properties of the olfactory receptor sequences. It is remarkable that the diverse approaches summarized here have yielded largely convergent results. The next stage in studies of this fascinating family of molecules should produce critical evidence for the regulatory mechanisms involved in gene expression, and identification of residue motifs specific to the binding pockets of different receptors, providing the basis for a receptor classification on functional grounds. This information will need to be integrated with the results of a wealth of studies of odor maps and neuronal circuits in the olfactory pathway before an understanding of the brain mechanisms underlying smell perception can begin to emerge.

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To download media files, please first review and agree to the Terms of Use. Download a photo or video by clicking or tapping on it. To download all photos or videos related to this article, select the links at the bottom of each section.

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