A set of SNARE proteins in the contractile vacuole complex of Paramecium regulates cellular calcium tolerance and also contributes to organelle biogenesis

Schönemann, Barbara; Bledowski, Alexander; Sehring, Ivonne Margarete; Plattner, Helmut

doi:10.1016/j.ceca.2012.11.016

Cited by 17 publications

(23 citation statements)

References 82 publications

(36 reference statements)

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“…But whether alveoli are related to the endoplasmic reticulum, or share more general structural or functional features, has not yet been thoroughly investigated. Similarly, there are remarkably few molecular data to aid in understanding the membrane trafficking aspects of the contractile vacuole or its evolutionary origins, though some compartment‐specific SNAREs and Rabs have been identified . The contractile vacuole is a highly dynamic organelle that shows markedly different organization even between Tetrahymena and Paramecium , whose water‐pumping activity is essential for ciliates and other fresh water protists lacking cell walls.…”

Section: Looking Aheadmentioning

confidence: 99%

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

Guerrier

Plattner

Richardson

et al. 2016

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As most of eukaryotic diversity lies in single-celled protists, they represent unique opportunities to ask questions about the balance of conservation and innovation in cell biological features. Among free-living protists the ciliates offer ease of culturing, a rich array of experimental approaches, and versatile molecular tools, particularly in Tetrahymena thermophila and Paramecium tetraurelia. These attributes have been exploited by researchers to analyze a wealth of cellular structures in these large and complex cells. This mini-review focuses on three aspects of ciliate membrane dynamics, all linked with endolysosomal trafficking. First is nutrition based on phagocytosis and maturation of food vacuoles. Secondly, we discuss regulated exocytosis from vesicles that have features of both dense core secretory granules but also lysosome-related organelles. The third topic is the targeting, breakdown and resorption of parental nuclei in mating partners. For all three phenomena, it is clear that elements of the canonical membrane-trafficking system have been retained and in some cases repurposed. In addition, there is evidence that recently evolved, lineage-specific proteins provide determinants in these pathways.

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Section: Looking Aheadmentioning

confidence: 99%

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

Guerrier

Plattner

Richardson

et al. 2016

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“…Moreover, it has been shown that acidocalcisomes can come into intimate contact with the contractile vacuole in Dictyostelium (Marchesini et al 2002) and in Trypanosoma (Rohloff and Docampo 2008). Again such knowledge is not available for Paramecium although its contractile vacuole complex is of paramount importance for regulating [Ca 2+ ] i homeostasis (Stock et al 2002;Plattner et al 2012;Sch€ onemann et al 2013). Here, localization studies (Wright and van Houten 1990) did not aim at showing Ca 2+ -ATPase in the contractile vacuole complex and cilia were also negative.…”

Section: Organelles Serving As Ca 2+ Storesmentioning

confidence: 82%

“…; Schönemann et al. ). Here, localization studies (Wright and van Houten ) did not aim at showing Ca 2+ ‐ATPase in the contractile vacuole complex and cilia were also negative.…”

Section: Capabilities Of Ca2+ Signaling From Paramecium To Manmentioning

confidence: 99%

“…Concomitantly silencing of contractile vacuole complex‐resident SNAREs greatly increases the sensitivity to even moderately increased [Ca 2+ ] o (Schönemann et al. ). Similarly, inhibition of the organellar H + ‐ATPase compromises cells in their vitality after increasing [Ca 2+ ] o (Sehring et al.…”

Section: Focusing Still More On Details Specific For Parameciummentioning

confidence: 99%

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Calcium Regulation in the Protozoan Model, Paramecium tetraurelia

Plattner

2013

J Eukaryotic Microbiology

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Early in eukaryotic evolution, the cell has evolved a considerable inventory of proteins engaged in the regulation of intracellular Ca(2+) concentrations, not only to avoid toxic effects but beyond that to exploit the signaling capacity of Ca(2+) by small changes in local concentration. Among protozoa, the ciliate Paramecium may now be one of the best analyzed models. Ciliary activity and exo-/endocytosis are governed by Ca(2+) , the latter by Ca(2+) mobilization from alveolar sacs and a superimposed store-operated Ca(2+) -influx. Paramecium cells possess plasma membrane- and endoplasmic reticulum-resident Ca(2+) -ATPases/pumps (PMCA, SERCA), a variety of Ca(2+) influx channels, including mechanosensitive and voltage-dependent channels in the plasma membrane, furthermore a plethora of Ca(2+) -release channels (CRC) of the inositol 1,4,5-trisphosphate and ryanodine receptor type in different compartments, notably the contractile vacuole complex and the alveolar sacs, as well as in vesicles participating in vesicular trafficking. Additional types of CRC probably also occur but they have not been identified at a molecular level as yet, as is the equivalent of synaptotagmin as a Ca(2+) sensor for exocytosis. Among established targets and sensors of Ca(2+) in Paramecium are calmodulin, calcineurin, as well as Ca(2+) /calmodulin-dependent protein kinases, all with multiple functions. Thus, basic elements of Ca(2+) signaling are available for Paramecium.

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“…First, they may serve for fine-tuning of Ca 2+ secretion (Ladenburger et al , 2006) similar to systemic functions in kidney. Second, they may provide Ca 2+ for local restructuring of the spongiome by reversible fusion and fission processes by the numerous organelle-specific SNARE proteins (Schönemann et al , 2013). This may enable the adjustment of organelle structure and function to the actual physiological requirements (Plattner, 2013).…”

Section: Intracellular Calcium Channels In Ciliatesmentioning

confidence: 99%

Intracellular calcium channels in protozoa

Docampo¹,

Moreno²,

Plattner³

2014

European Journal of Pharmacology

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Ca2+-signaling pathways and intracellular Ca2+ channels are present in protozoa. Ancient origin of inositol 1,4,5-trisphosphate receptors (IP3Rs) and other intracellular channels predates the divergence of animals and fungi as evidenced by their presence in the choanoflagellate Monosiga brevicollis, the closest known relative to metazoans. The first protozoan IP3R cloned, from the ciliate Paramecium, displays strong sequence similarity to the rat type 3 IP3R. This ciliate has a large number of IP3- and ryanodine(Ry)-like receptors in 6 subfamilies suggesting the evolutionary adaptation to local requirements for an expanding diversification of vesicle trafficking. IP3Rs have also been functionally characterized in trypanosomatids, where they are essential for growth, differentiation, and establishment of infection. The presence of the mitochondrial calcium uniporter (MCU) in a number of protozoa indicates that mitochondrial regulation of Ca2+ signaling is also an early appearance in evolution, and contributed to the discovery of the molecular nature of this channel in mammalian cells. There is only sequence evidence for the occurrence of two-pore channels (TPCs), transient receptor potential Ca2+ channels (TRPCs) and intracellular mechanosensitive Ca2+-channels in Paramecium and in parasitic protozoa.

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A set of SNARE proteins in the contractile vacuole complex of Paramecium regulates cellular calcium tolerance and also contributes to organelle biogenesis

Cited by 17 publications

References 82 publications

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

Calcium Regulation in the Protozoan Model, Paramecium tetraurelia

Intracellular calcium channels in protozoa

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