Mechanisms underlying dual effects of serotonin during development of Helisoma trivolvis (Mollusca)

BMC Developmental Biology

Evgeni G Ponimaskin²  Leonid P Nezlin¹  Evgeny Ivashkin³  Marina Yu Khabarova¹  Elena E Voronezhskaya¹  Konstantin Glebov⁴ 

[1]Institute of Developmental Biology RAS, Moscow, Russia

[2]Department of Cellular Neurophysiology, Carl-Neuberg-Str. 1, 30625 Hannover, Germany

[3]Department of Experimental Neurocytology, Brain Research Branch, Scientific Center of Neurology, RAMS, Moscow, Russia

[4]DFG-Research Center Molecular Physiology of the Brain (CMPB), Göttingen, Germany

关键词: Larval competence;    Trochophore;    Metamorphosis;    Development;    Helisoma trivolvis;    Serotonin receptors;   

Others  :  1085026
DOI  :  10.1186/1471-213X-14-14

 received in 2013-11-16, accepted in 2014-02-21,  发布年份 2014

【 摘 要 】

Background

Serotonin (5-HT) is well known as widely distributed modulator of developmental processes in both vertebrates and invertebrates. It is also the earliest neurotransmitter to appear during neuronal development. In aquatic invertebrates, which have larvae in their life cycle, 5-HT is involved in regulation of stages transition including larval metamorphosis and settlement. However, molecular and cellular mechanisms underlying developmental transition in aquatic invertebrate species are yet poorly understood. Earlier we demonstrated that in larvae of freshwater molluscs and marine polychaetes, endogenous 5-HT released from the neurons of the apical sensory organ (ASO) in response to external stimuli retarded larval development at premetamorphic stages, and accelerated it at metamorphic stages. Here we used a freshwater snail Helisoma trivolvis to study molecular mechanisms underlying these dual developmental effects of 5-HT.

Results

Larval development of H. trivolvis includes transition from premetamorphic to metamorphic stages and shares the main features of metamorphosis with free-swimming aquatic larvae. Three types of 5-HT receptors (5-HT₁-, 5-HT₄- and 5-HT₇-like) are functionally active at premetamorphic (trochophore, veliger) and metamorphic (veliconcha) stages, and expression patterns of these receptors and respective G proteins undergo coordinated changes during development. Stimulation of these receptors modulated cAMP-dependent regulation of cell divisions. Expression of 5-HT₄- and 5-HT₇-like receptors and their downstream G_s protein was down-regulated during the transition of pre- to metamorphic stage, while expression of 5-HT₁ -like receptor and its downstream G_i protein was upregulated. In accordance with relative amount of these receptors, stimulation of 5-HTRs at premetamorphic stages induces developmental retardation, while their stimulation at metamorphic stages induces developmental acceleration.

Conclusions

We present a novel molecular mechanism that underlies stage-specific changes in developmental tempo of H. trivolvis larvae in response to endogenous 5-HT produced by the neurons of the ASO. We suggest that consecutive changes in expression patterns of different receptors and their downstream partners in the course of larval development represent the molecular base of larval transition from premetamorphic (non-competent) to metamorphic (competent) state.

【 授权许可】

   
2014 Glebov et al.; licensee BioMed Central Ltd.

【 图 表 】

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