Hussain, Ashiq
(2010).
The teleost taar family of olfactory receptors: From rapidly evolving receptor genes to ligand-induced behavior.
PhD thesis, Universität zu Köln.
Abstract
Trace amine-associated receptors (TAARs) have recently been shown to function as olfactory receptors in mammals. In this current study, the taar gene family has been delineated in jawless, cartilaginous, and bony fish (zero, 2, and >100 genes, respectively). I conclude that the taar genes are evolutionary much younger than the related OR and ORA/V1R olfactory receptor families, which are present already in lamprey, a jawless vertebrate. The 2 cartilaginous fish genes appear to be ancestral for 2 taar classes, each with mammalian and bony fish (teleost) representatives. Unexpectedly, a whole new clade, class III, of taar genes originated even later, within the teleost lineage. Taar genes from all 3 classes are expressed in subsets of zebrafish olfactory receptor neurons, supporting their function as olfactory receptors. The highly conserved TAAR1 (shark,mammalian, and teleost orthologs) is not expressed in the olfactory epithelium and may constitute the sole remnant of a primordial, non olfactory function of this family. Class III comprises three-fourths of all teleost taar genes and is characterized by the complete loss of the aminergic ligand-binding motif, stringently conserved in all 25 genes of the other 2 classes. Two independent intron gains in class III taar genes represent extraordinary evolutionary dynamics, considering the virtual absence of intron gains during vertebrate evolution. The dN/dS analysis suggests both minimal global negative selection and an unparalleled degree of local positive selection as another hallmark of class III genes. The accelerated evolution of class III teleost taar genes conceivably might mark the birth of another olfactory receptor gene family. Ligands have only been identified for a handful of olfactory receptors of mammals and insects, while only a single teleost olfactory receptor have been deorphanized, a member of the OlfC family, OlfCa. Zebrafish TAAR olfactory receptors of classI are good candidates for having amines as possible ligands, due to the presence of the aminergic ligand binding motifs. This study identifies diamines as specific ligands for a taar receptor, DrTAAR13c. These diamines activate a sparse subset of olfactory sensory neurons, as indicated by c-Fos expression in olfactory epithelium. Diamines, putrescine and cadaverine, are foul-smelling aliphatic polycations that occur naturally as a result of bacterial decarboxylation of amino acids lysine and arginine, respectively. The 15 concentration of diamines in their environment is correlated to the degree of putrefication. In the behavioral assay, zebrafish exposed to even low concentration of diamines show dramatic, quantifiable aversion, while it shows attraction towards food stimulus and no response for water. The ligand spectrum of TAAR13c closely parallels the behavioral effectiveness of these diamines. This data is consistent with the existence of a defined neuronal microcircuit that elicits a characteristic behavior upon activation of a single olfactory receptor, a novum in the vertebrate sense of smell.
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