Calcium signalling in the ciliated protozoan model, Paramecium : Strict signal localisation by epigenetically controlled positioning of different Ca²⁺-channels

Abstract

The Paramecium tetraurelia cell is highly organised, with regularly spaced elements pertinent to Ca2+ signalling under epigenetic control. Vesicles serving as stationary Ca2+ stores or undergoing trafficking contain Ca2+-release channels (PtCRCs) which, according to sequence and domain comparison, are related either to inositol 1,4,5-trisphosphate (InsP3) receptors (IP3R) or to ryanodine receptor-like proteins (RyR-LP) or to both, with intermediate characteristics or deviation from conventional domain structure. Six groups of such PtCRCs have been found. The ryanodine-InsP3-receptor homology (RIH) domain is not always recognisable, in contrast to the channel domain with six trans-membrane domains and the pore between transmembrane domain 5 and 6. Two CRC subtypes tested more closely, PtCRC-II and PtCRC-IV, with and without an InsP3-binding domain, reacted to InsP3 and to caffeine, respectively, and hence represent IP3Rs and RyR-LPs. IP3Rs occur in the contractile vacuole complex where they allow for stochastic constitutive Ca2+ reflux into the cytosol. RyR-LPs are localised to cortical Ca2+ stores; they are engaged in dense core-secretory vesicle exocytosis by Ca2+ release, superimposed by Ca2+-influx via non-ciliary Ca2+-channels. One or two different types of PtCRCs also occur in other vesicles undergoing trafficking. Since the PtCRCs described combine different features they are considered derivatives of primitive precursors. The highly regular, epigenetically controlled design of a Paramecium cell allows it to make Ca2+ available very locally, in a most efficient way, along predetermined trafficking pathways, including regulation of exocytosis, endocytosis, phagocytosis and recycling phenomena. The activity of cilia is also regulated by Ca2+, yet independently from any CRCs, by de- and hyperpolarisation of the cell membrane potential.