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First published online December 1, 2006
Journal of Experimental Biology 209, 4858-4868 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02607
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Ancestry of neuronal monoamine transporters in the Metazoa

Stanley Caveney1,*, Wendy Cladman1, LouAnn Verellen2 and Cam Donly2

1 Department of Biology, University of Western Ontario, London, ON, Canada N6A 5B7
2 Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, London, ON, Canada N5V 4T3

* Author for correspondence (e-mail: caveney{at}uwo.ca)

Accepted 18 October 2006

Selective Na+-dependent re-uptake of biogenic monoamines at mammalian nerve synapses is accomplished by three types of solute-linked carrier family 6 (SLC6) membrane transporter with high affinity for serotonin (SERTs), dopamine (DATs) and norepinephrine (NETs). An additional SLC6 monoamine transporter (OAT), is responsible for the selective uptake of the phenolamines octopamine and tyramine by insect neurons. We have characterized a similar high-affinity phenoloamine transporter expressed in the CNS of the earthworm Lumbricus terrestris. Phylogenetic analysis of its protein sequence clusters it with both arthropod phenolamine and chordate catecholamine transporters. To clarify the relationships among metazoan monoamine transporters we identified representatives in the major branches of metazoan evolution by polymerase chain reaction (PCR)-amplifying conserved cDNA fragments from isolated nervous tissue and by analyzing available genomic data. Analysis of conserved motifs in the sequence data suggest that the presumed common ancestor of modern-day Bilateria expressed at least three functionally distinct monoamine transporters in its nervous system: a SERT currently found throughout bilaterian phyla, a DAT now restricted in distribution to protostome invertebrates and echinoderms and a third monoamine transporter (MAT), widely represented in contemporary Bilateria, that is selective for catecholamines and/or phenolamines. Chordate DATs, NETs, epinephrine transporters (ETs) and arthropod and annelid OATs all belong to the MAT clade. Contemporary invertebrate and chordate DATs belong to different SLC6 clades. Furthermore, the genes for dopamine and norepinephrine transporters of vertebrates are paralogous, apparently having arisen through duplication of an invertebrate MAT gene after the loss of an invertebrate-type DAT gene in a basal protochordate.

Key words: Bilateria, protostome, deuterostome, monoamine, neurotransmitters, transporter, SLC6 family, octopamine, tyramine, dopamine, norepinephrine, serotonin, earthworm, Lumbricus terrestris






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