Ca2+ signalling early in evolution – all but primitive

2015

Cell Calcium

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The ciliated protozoan, Paramecium tetraurelia has a high basic Ca(2+) leakage rate which is counteracted mainly by export through a contractile vacuole complex, based on its V-type H(+)-ATPase activity. In addition Paramecium cells dispose of P-type Ca(2+)-ATPases, i.e. a plasmamembrane and a sarcoplasmic/endoplasmic reticulum Ca(2+)-ATPase (PMCA, SERCA). Antiporter systems are to be expected, as inferred from indirect evidence. Among the best known cytosolic Ca(2+)-binding proteins, calmodulin activates Ca(2+) influx channels in the somatic cell membrane, but inactivates Ca(2+) influx channels in cilia, where it, thus, ends ciliary reversal induced by depolarization via channels in the somatic cell membrane. Centrin inactivates Ca(2+) signals after stimulation by its high capacity/low affinity binding sites, whereas its high affinity sites regulate some other functions. Cortical Ca(2+) stores (alveolar sacs) are activated during stimulated trichocyst exocytosis and thereby mediate store-operated Ca(2+) entry (SOCE). Ca(2+) release channels (CRCs) localised to alveoli and underlying SOCE are considered as Ryanodine receptor-like proteins (RyR-LPs) which are members of a CRC family with 6 subfamilies. These also encompass genuine inositol 1,4,5-trisphosphate receptors (IP3Rs) and intermediates between the two channel types. All IP3R/RyR-type CRCs possess six carboxyterminal transmembrane domains (TMD), with a pore domain between TMD 5 and 6, endowed with a characteristic selectivity filter. There are reasons to assume a common ancestor molecule for such channels and diversification further on in evolution. The distinct distribution of specific CRCs in the different vesicles undergoing intracellular trafficking suggests constitutive formation of very locally restricted Ca(2+) signals during vesicle-vesicle interaction. In summary, essential steps of Ca(2+) signalling already occur at this level of evolution, including an unexpected multitude of CRCs. For dis-/similarities with other bikonts see "Conclusions".

Section: Mixed Types Of Crcs and Common Originmentioning

confidence: 87%

Molecular aspects of calcium signalling at the crossroads of unikont and bikont eukaryote evolution – The ciliated protozoan Paramecium in focus

2015

Cell Calcium

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“…6 transmembrane domains, for the skeletal muscle RyR [97] and this now seems to be tacitly accepted also by others [98]. Furthermore, the general assignment of a sequence Gly-Val-GlyAsp to the selectivity filter of IP 3 Rs and Gly-Ile-Gly-Asp to that of RyRs [99] is not applicable to lower eukaryotes; not only CRCs of Paramecium [28], but also those in lower metazoans show these two motives alternatively [12].…”

Section: The Pore Region Of the Ptcrcs Molecules In Comparison To Mammentioning

confidence: 94%

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

2015

Cell Calcium

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The Paramecium tetraurelia cell is highly organised, with regularly spaced elements pertinent to Ca(2+) signalling under epigenetic control. Vesicles serving as stationary Ca(2+) stores or undergoing trafficking contain Ca(2+)-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 Ca(2+) reflux into the cytosol. RyR-LPs are localised to cortical Ca(2+) stores; they are engaged in dense core-secretory vesicle exocytosis by Ca(2+) release, superimposed by Ca(2+)-influx via non-ciliary Ca(2+)-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 Ca(2+) 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 Ca(2+), yet independently from any CRCs, by de- and hyperpolarisation of the cell membrane potential.

“…Vesicles undergoing trafficking are endowed with CRCs identical with, or related to InsP 3 Rs and RyRs (Ladenburger and Plattner 2011;Plattner and Verkhratsky 2013); see Box 5. An exception are trichocysts which seem to be devoid of luminal Ca 2+ , in contrast to what is known from some other dense core-secretory vesicles, endosomes and phagocytotic organelles of higher eukaryotes (Hay 2007).…”

Section: Molecular Backgroundmentioning

confidence: 99%

“…The Ca 2+ signal is generated by intracellular CRCs of which different types are assigned to different organelles (Ladenburger and Plattner 2011;Plattner and Verkhratsky 2013). The Ca 2+ -sensor causing fusion, as known from higher eukaryotes, is a low capacity/high affinity Ca 2+ -binding protein (CaBP) which usually contains two high affinity Ca 2+ -binding C2 domains (β-barrels with a Ca 2+ -binding loop), such as synaptotagmin (Rizo et al 2006;Südhof 2014).…”

mentioning

confidence: 99%

Principles of Intracellular Signaling in Ciliated Protozoa—A Brief Outline

Biocommunication of Ciliates

2016

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Ciliates have available most of the intracellular signaling mechanisms known from metazoans. Long-range signals are represented by firmly installed microtubules serving as gliding rails aiming at specific targets. Many components are distinctly arranged to guarantee locally restricted effects. Short-range signals include Ca 2+ , provided from different sources, and proteins for membrane recognition and fusion, such as SNAREs, GTPases and high affinity Ca 2+ -binding proteins (still to be defined). A battery of ion conductances serves for electric coupling from the outside medium to specific responses, notably ciliary activity, which also underlies gravitaxis responses. Eventually cyclic nucleotides are involved, e.g. in ciliary signaling. Furthermore, an elaborate system of protein kinases and phosphatases exerts signaling mechanisms in widely different processes.