Identification, molecular structure and expression of two cloned serotonin receptors from the pond snail, <i>Helisoma trivolvis</i>

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SUMMARYAcceleration of embryonic rotation is a common response to hypoxia among pond snails. It was first characterized in Helisoma trivolvis embryos, which have a pair of sensorimotor neurons that detect hypoxia and release serotonin onto postsynaptic ciliary cells. The objective of the present study was to determine how the hypoxia response is mediated in Lymnaea stagnalis, which differ from H. trivolvis by having both serotonergic and dopaminergic neurons, and morphologically distinct ciliated structures at comparative stages of embryonic development. Time-lapse video recordings of the rotational behavior in L. stagnalis revealed similar rotational features to those previously observed in H. trivolvis, including rotational surges and rotational responses to hypoxia. Serotonin and dopamine increased the rate of rotation with similar potency. In contrast, serotonin was more potent than dopamine in stimulating the ciliary beat frequency of isolated pedal cilia. Isolated apical plate cilia displayed an irregular pattern of ciliary beating that precluded the measurement of ciliary beat frequency. A qualitative assessment of ciliary beating revealed that both serotonin and dopamine were able to stimulate apical plate cilia. The ciliary responses to dopamine were reversible in both pedal and apical plate cilia, whereas the responses to serotonin were only reversible at concentrations below 100mmol l -1 . Mianserin, a serotonin receptor antagonist, and SKF83566, a dopamine receptor antagonist, effectively blocked the rotational responses to serotonin and dopamine, respectively. The rotational response to hypoxia was only partially blocked by mianserin, but was fully blocked by SKF83566. These data suggest that, despite the ability of serotonin to stimulate ciliary beating in L. stagnalis embryos, the rotational response to hypoxia is primarily mediated by the transient apical catecholaminergic neurons that innervate the ciliated apical plate. Supplementary material available online at

Section: Characterization Of Pedal and Apical Plate Ciliasupporting

confidence: 54%

Section: Characterization Of Pedal and Apical Plate Ciliamentioning

confidence: 99%

Identification and evolutionary implications of neurotransmitter–ciliary interactions underlying the behavioral response to hypoxia inLymnaea stagnalisembryos

Goldberg

Rich

Muruganathan

et al. 2011

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“…These receptors, named 5-HT 1Hel and 5-HT 7Hel , respectively, are both expressed in embryonic ciliary cells, as well as in many neurons of the adult central nervous system (Mapara et al, 2008;Doran et al, 2004). A preliminary study of these suggested that 5-HT 1Hel receptors probably mediate a transient large-amplitude cilioexcitatory response to serotonin (Gallin et al, 2006).…”

Section: Embryonic Rotational Behaviour and The Underlying Physiologimentioning

confidence: 99%

Integrative biology of an embryonic respiratory behaviour in pond snails:the `embryo stir-bar hypothesis'

Goldberg

Doran

Shartau

et al. 2008

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SummaryEmbryos of freshwater snails undergo direct development from single cell to juvenile inside egg masses that are deposited on vegetation and other substratum in pond, lake and stream habitats. Helisoma trivolvis, a member of the Planorbidae family of basommatophoran snails, has served as a model for studying the developmental and physiological roles for neurotransmitters during embryogenesis. Early studies revealed that H. trivolvis embryos from stage E15 to E30, the period between gastrulation and the trochophore-juvenile transition, display a cilia-driven behaviour consisting of slow basal rotation and transient periods of rapid rotation. The discovery of a bilateral pair of early serotonergic neurons, named ENC1, which project an apical process to the embryo surface and basal neurites to ciliated cells, prompted the hypothesis that each ENC1 is a dual-function sensory and motor neuron mediating a physiological embryonic response. This article reviews our past and present studies and addresses questions concerning this hypothesis, including the following. (1) What environmental signal regulates ENC1 activity and rotational behaviour? (2) Does ENC1 function as both a primary sensory and motor neuron underlying the rotational behaviour? (3) What are the sensory transduction mechanisms? (4) How does ENC1 regulate ciliary beating? (5) Do other basommatophoran species have similar neural-ciliary pathways and behavioural responses? (6) How is the behaviour manifest in the dynamic natural environment? In this review, we introduce the 'embryo stir-bar hypothesis', which proposes that embryonic rotation is a hypoxiasensitive respiratory behaviour responsible for mixing the egg capsule fluid, thereby enhancing delivery of environmental oxygen to the embryo.

“…Mianserin acts on the 5-HT-type II (5HT 2 ) receptor; however, whether this receptor is present in H. trivolvis embryos is unknown as only the 5-HT-type I H. trivolvis (5-HT 1Hel ) and 5-HT-type VII H. trivolvis (5-HT 7Hel ) receptors have been identified (Mitchell et al, 1990;Csaba et al, 2003;Mapara et al, 2008). It is difficult to conclude from the actions of mianserin that the 5-HT 2 receptor is present because of its poor specificity and the unreliability of transferring pharmacological profiles of vertebrate receptors to their invertebrate counterparts (Goldberg et al, 1994;HaySchmidt, 2000;Mapara et al, 2008).…”

Section: Energy Regulation Through a 5-ht Pathwaymentioning

confidence: 99%

“…It is difficult to conclude from the actions of mianserin that the 5-HT 2 receptor is present because of its poor specificity and the unreliability of transferring pharmacological profiles of vertebrate receptors to their invertebrate counterparts (Goldberg et al, 1994;HaySchmidt, 2000;Mapara et al, 2008). It appears that mianserin is an effective antagonist on whichever receptor is linked to acute 5-HT-stimulated rotation.…”

Section: Energy Regulation Through a 5-ht Pathwaymentioning

confidence: 99%

Serotonin prolongs survival of encapsulated pond snail embryos exposed to long-term anoxia

Shartau

Tam

Patrick

et al. 2010

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SUMMARY Embryos of the pond snail, Helisoma trivolvis, develop bilateral serotonergic neurons that innervate ciliary bands and stimulate cilia-driven rotation. This behaviour is postulated to increase oxygen availability during hypoxia by mixing the capsular fluid. We hypothesised that the stimulation of ciliary-driven rotation by serotonin (5-HT) enhances the survival of embryos during prolonged hypoxia. Embryo rotation and survival were monitored in different levels of oxygen for 24–48 h while in the presence or absence of 5-HT (100 μmol l−1) or a 5-HT antagonist (50 μmol l−1). Long-term hypoxia caused delayed embryonic development that appeared morphologically normal. Hypoxia also induced a transient increase in rotation rate in embryos exposed to artificial pond water (APW) or 5-HT that lasted around 3 h. 5-HT-treated embryos had an elevated rotation rate over embryos in APW throughout the long-term exposure to hypoxia. Long-term anoxia also induced a transient increase in rotation rate in embryos exposed to APW or 5-HT. Rotation ceased in embryos exposed to APW by 13 h but persisted in 5-HT-treated embryos for up to 40 h. Fifty percent mortality was reached at 9 h of anoxia in embryos in APW and at 24 h in 5-HT-treated embryos. The 5-HT antagonist mianserin partially inhibited the 5-HT enhancement of rotation but not the prolongation of survival in anoxia. The ability of 5-HT to prolong survival in anoxia reveals a 5-HT-activated metabolic pathway that liberates an alternative energy source.