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Proc Natl Acad Sci U S A. 2017 Jul 11;114(28):7397-7402. doi: 10.1073/pnas.1704009114. Epub 2017 Jun 26.

Evolution of immune chemoreceptors into sensors of the outside world.

Author information

1
Department of Genetics and Evolution, University of Geneva, Geneva 1205, Switzerland.
2
Geneva Neuroscience Center, University of Geneva, Geneva 1205, Switzerland.
3
Department of Mammalogy and Ornithology, Natural History Museum of Geneva, Geneva 1208, Switzerland.
4
Geneva Neuroscience Center, University of Geneva, Geneva 1205, Switzerland; alan.carleton@unige.ch ivan.rodriguez@unige.ch.
5
Department of Basic Neurosciences, School of Medicine, University of Geneva, Geneva 1205, Switzerland.
6
Department of Genetics and Evolution, University of Geneva, Geneva 1205, Switzerland; alan.carleton@unige.ch ivan.rodriguez@unige.ch.

Abstract

Changes in gene expression patterns represent an essential source of evolutionary innovation. A striking case of neofunctionalization is the acquisition of neuronal specificity by immune formyl peptide receptors (Fprs). In mammals, Fprs are expressed by immune cells, where they detect pathogenic and inflammatory chemical cues. In rodents, these receptors are also expressed by sensory neurons of the vomeronasal organ, an olfactory structure mediating innate avoidance behaviors. Here we show that two gene shuffling events led to two independent acquisitions of neuronal specificity by Fprs. The first event targeted the promoter of a V1R receptor gene. This was followed some 30 million years later by a second genomic accident targeting the promoter of a V2R gene. Finally, we show that expression of a vomeronasal Fpr can reverse back to the immune system under inflammatory conditions via the production of an intergenic transcript linking neuronal and immune Fpr genes. Thus, three hijackings of regulatory elements are sufficient to explain all aspects of the complex expression patterns acquired by a receptor family that switched from sensing pathogens inside the organism to sensing the outside world through the nose.

KEYWORDS:

gene evolution; neofunctionalization; olfaction; olfactory receptor; vomeronasal organ

PMID:
28652375
PMCID:
PMC5514743
DOI:
10.1073/pnas.1704009114
[Indexed for MEDLINE]
Free PMC Article

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