Histamine is a modulator of metamorphic competence in Strongylocentrotus purpuratus (Echinodermata: Echinoidea)

BMC Developmental Biology

Andreas Heyland²  Mariana Leguia³  Gary Wessel¹  Julia Nguyen²  Jamie-Lee Giardini²  Josh Sutherby² 

[1] Brown University, MCB, Providence, RI 02912, USA;University of Guelph, Integrative Biology, Guelph, ON N1G-2 W1, Canada;Current address: U.S. Naval Medical Research Unit No.6, Lima, Peru

关键词: Modulation;    Life history evolution;    Settlement;    Histamine receptors;    Histamine;    Echinoderm life-history;    Settlement;    Metamorphic competence;    Metamorphosis;   

Others  :  1086651
DOI  :  10.1186/1471-213X-12-14

 received in 2011-11-30, accepted in 2012-03-13,  发布年份 2012

【 摘 要 】

Background

A metamorphic life-history is present in the majority of animal phyla. This developmental mode is particularly prominent among marine invertebrates with a bentho-planktonic life cycle, where a pelagic larval form transforms into a benthic adult. Metamorphic competence (the stage at which a larva is capable to undergo the metamorphic transformation and settlement) is an important adaptation both ecologically and physiologically. The competence period maintains the larval state until suitable settlement sites are encountered, at which point the larvae settle in response to settlement cues. The mechanistic basis for metamorphosis (the morphogenetic transition from a larva to a juvenile including settlement), i.e. the molecular and cellular processes underlying metamorphosis in marine invertebrate species, is poorly understood. Histamine (HA), a neurotransmitter used for various physiological and developmental functions among animals, has a critical role in sea urchin fertilization and in the induction of metamorphosis. Here we test the premise that HA functions as a developmental modulator of metamorphic competence in the sea urchin Strongylocentrotus purpuratus.

Results

Our results provide strong evidence that HA leads to the acquisition of metamorphic competence in S. purpuratus larvae. Pharmacological analysis of several HA receptor antagonists and an inhibitor of HA synthesis indicates a function of HA in metamorphic competence as well as programmed cell death (PCD) during arm retraction. Furthermore we identified an extensive network of histaminergic neurons in pre-metamorphic and metamorphically competent larvae. Analysis of this network throughout larval development indicates that the maturation of specific neuronal clusters correlates with the acquisition of metamorphic competence. Moreover, histamine receptor antagonist treatment leads to the induction of caspase mediated apoptosis in competent larvae.

Conclusions

We conclude that HA is a modulator of metamorphic competence in S. purpuratus development and hypothesize that HA may have played an important role in the evolution of settlement strategies in echinoids. Our findings provide novel insights into the evolution of HA signalling and its function in one of the most important and widespread life history transitions in the animal kingdom - metamorphosis.

【 授权许可】

   
2012 Sutherby et al.; licensee BioMed Central Ltd.

【 图 表 】

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