Characterization of a Novel Serotonin Receptor from
Caenorhabditis elegans: Cloning and Expression
of Two Splice Variants
Fadi F. Hamdan, *Mark D. Ungrin, *Mark Abramovitz, and Paula Ribeiro
Institute of Parasitology, McGill University, Ste. Anne de Bellevue; and *Department of Biochemistry and Molecular Biology,
Merck Frosst Centre for Therapeutic Research, Pointe Claire-Dorval, Quebec, Canada
Abstract: Serotonin [5-hydroxytryptamine (5-HT)] modu-
lates feeding activity, egg-laying, and mating behavior in
the free-living nematode, Caenorhabditis elegans. We
have cloned a novel receptor cDNA from C. elegans
(5-HT
2Ce
) that has high sequence homology with 5-HT
2
receptors from other species. When transiently ex-
pressed in COS-7 cells, 5-HT
2Ce
exhibited 5-HT binding
activity and activated Ca
2+
-mediated signaling in a man-
ner analogous to other 5-HT
2
receptors. However,
5-HT
2Ce
displayed unusual pharmacological properties,
which resembled both 5-HT
2
and 5-HT
1
-like receptors
but did not correlate well with any of the known 5-HT
2
subtypes. Two splice variants of 5-HT
2Ce
that differ by 48
N-terminal amino acids were identified. The two isoforms
were found to have virtually identical binding and signal-
ing properties but differed in their levels of mRNA expres-
sion, with the longer variant being four times more abun-
dant than the shorter species in all developmental stages
tested. Taken together, the results describe two variants
of a novel C. elegans 5-HT receptor, which has some of
the properties of the 5-HT
2
family but whose pharmaco-
logical profile does not conform to any known class of
receptor. Key Words: Caenorhabditis elegans—Seroto-
nin—5-HT
2
receptor—G protein-coupled receptor—
Cloning—Expression—Spliced leader—Aequorin.
J. Neurochem. 72, 1372–1383 (1999).
Serotonin [5-hydroxytryptamine (5-HT)] is a widely
distributed neuroactive agent of vertebrates and inverte-
brates. In the free-living nematode Caenorhabditis el-
egans, 5-HT has been identified within several central
and peripheral neurons, including the well-characterized
pharyngeal neurosecretory motorneurons, the hermaph-
rodite-specific neurons, and the male-specific CP neu-
rons (Horvitz et al., 1982; Desai et al., 1988; Loer and
Kenyon, 1993). The serotonergic neurosecretory motor
neurons may modulate pharyngeal pumping (feeding),
locomotion, and egg laying, whereas the hermaphrodite-
specific neurons and CP neurons seem to affect egg-
laying and male mating behavior, respectively (Horvitz
et al., 1982; Desai and Horvitz, 1989; Loer and Kenyon,
1993). These effects of 5-HT are mediated, in part, by G
proteins (Bargmann and Kaplan, 1998) and at least one
type of G protein-coupled receptor (GPCR), which is
negatively linked to adenylate cyclase (Olde and Mc-
Combie, 1997). It is unknown at present if there are other
receptors and pathways of signal transduction that me-
diate the multiple effects of 5-HT in this animal.
In mammals, where 5-HT is a well-established neuro-
transmitter involved in a wide range of physiological
activities (Leonard, 1994), as many as seven different
classes of 5-HT receptors (5-HT
1
–5-HT
7
) have been
identified, all of which are further divided into multiple
subtypes (Hoyer et al., 1994; Gerhardt and Van Heer-
ikhuizen, 1997). The vast majority of mammalian 5-HT
receptors belong to the large GPCR superfamily and
couple to adenylate cyclase, either positively (5-HT
4
,
5-HT
6
, and 5-HT
7
) or negatively (5-HT
1
). In contrast, the
5-HT
2
family has very distinctive structural properties
and couples to phospholipase C and the phosphoinositol
(inositol trisphosphate)/Ca
2+
-mediated pathway of sig-
nal transduction (Hoyer et al., 1994; Gerhardt and Van
Heerikhuizen, 1997).
Received October 15, 1998; revised manuscript received November
30, 1998; accepted December 7, 1998.
Address correspondence and reprint requests to Dr. P. Ribeiro at
Institute of Parasitology, McGill University, Macdonald Campus, 21,
111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, Canada H9X
3V9.
Abbreviations used: CeIF, Caenorhabditis elegans eukaryotic initi-
ation factor 4A homologue; DOI, 2,5-dimethoxy-4-iodoamphetamine;
GPCR, G protein-coupled receptor; 5-HT, 5-hydroxytryptamine (sero-
tonin); 5-HT
Asc
, putative 5-hydroxytryptamine
2
-like sequence recently
cloned from the parasitic nematode Ascaris suum; 5-HT
2Ce
, 5-hydroxy-
tryptamine
2
receptor from Caenorhabditis elegans; 5-HT
2CeL
and
5-HT
2CeS
, long and short, respectively, 5-hydroxytryptamine
2
receptor
isoform from Caenorhabditis elegans; 5-HT
2Dro
, 5-hydroxytrypta-
mine
2
receptor cloned from Drosophila; 5-HT
2Lym
, 5-hydroxytrypta-
mine
2
receptor cloned from the pond snail, Lymnaea; LSD, lysergic
acid diethylamide; 8-OH-DPAT, 8-hydroxy-2-(di-n-propylamino)tetra-
lin; ORF, open reading frame; PBS, phosphate-buffered saline; RACE,
rapid amplification of cDNA ends; SL, spliced leader; TEM buffer, 50
mM Tris (pH 7.4), 0.5 mM EDTA, and 10 mM MgCl
2
; TM, transmem-
brane domain; UTR, untranslated region.
1372
Journal of Neurochemistry
Lippincott Williams & Wilkins, Inc., Philadelphia
© 1999 International Society for Neurochemistry