Conservation and Innovation in Tetrahymena Membrane Traffic: Proteins, Lipids, and Compartments

Nusblat, Alejandro D.; Bright, Lydia J.; Turkewitz, Aaron P.

doi:10.1016/b978-0-12-385967-9.00006-2

Cited by 23 publications

(23 citation statements)

References 127 publications

(173 reference statements)

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“…One hint is that wortmannin, which inhibits the formation of PI 3‐phosphate, affects secretion of hydrolytic enzymes in T. thermophila , and the effect may be at the level of phagosome maturation . This phenomenon is ripe for analysis, since Tetrahymena appear to synthesize most but not all of the phosphorylated PI derivatives made in mammalian cells, and the PI interconverting enzymes have been identified . Thus, ciliates appear to offer promising systems to illuminate evolutionary aspects of lipid‐based protein targeting, particularly with regard to the phagosomal pathway.…”

Section: Food Uptake and The Phagocytic Pathwaymentioning

confidence: 99%

“…59 This phenomenon is ripe for analysis, since Tetrahymena appear to synthesize most but not all of the phosphorylated PI derivatives made in mammalian cells, and the PI interconverting enzymes have been identified. [60][61][62][63] Thus, ciliates appear to offer promising systems to illuminate evolutionary aspects of lipid-based protein targeting, particularly with regard to the phagosomal pathway.…”

Section: Food Uptake and The Phagocytic Pathwaymentioning

confidence: 99%

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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: Food Uptake and The Phagocytic Pathwaymentioning

confidence: 99%

Section: Food Uptake and The Phagocytic Pathwaymentioning

confidence: 99%

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

Guerrier

Plattner

Richardson

et al. 2016

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“…Around the cytoproct, small GTPases called RABs are abundant and localized. These have been considered as key determinants of compartmental specificity by recruiting endocytic structures to the cytoproct 68 . In mammals, RAB5 isoforms (RABA, B and C) are downstream of PtdIns3K signaling, which play roles as endosome organizers that transport a cargo from the plasma membrane to lysosomes 69 .…”

Section: Discussionmentioning

confidence: 99%

Role of class III phosphatidylinositol 3-kinase during programmed nuclear death ofTetrahymena thermophila

et al. 2013

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Programmed nuclear death (PND) in the ciliate protozoan Tetrahymena thermophila is a novel type of autophagy that occurs during conjugation, in which only the parental somatic macronucleus is destined to die and is then eliminated from the progeny cytoplasm. Other coexisting nuclei, however, such as new micro- and macronuclei are unaffected. PND starts with condensation in the nucleus followed by apoptotic DNA fragmentation, lysosomal acidification, and final resorption. Because of the peculiarity in the process and the absence of some ATG genes in this organism, the mechanism of PND has remained unclear. In this study, we focus on the role of class III phosphatidylinositol 3-kinase (PtdIns3K, corresponding to yeast Vps34) in order to identify central regulators of PND. We identified the sole Tetrahymena thermophila ortholog (TtVPS34) to yeast Vps34 and human PIK3C3 (the catalytic subunit of PtdIns3K), through phylogenetic analysis, and generated the gene knockdown mutant for functional analysis. Loss of TtVPS34 activity prevents autophagosome formation on the parental macronucleus, and this nucleus escapes from the lysosomal pathway. In turn, DNA fragmentation and final resorption of the nucleus are drastically impaired. These phenotypes are similar to the situation in the ATG8Δ mutants of Tetrahymena, implying an inextricable link between TtVPS34 and TtATG8s in controlling PND as well as general macroautophagy. On the other hand, TtVPS34 does not appear responsible for the nuclear condensation and does not affect the progeny nuclear development. These results demonstrate that TtVPS34 is critically involved in the nuclear degradation events of PND in autophagosome formation rather than with an involvement in commitment to the death program.

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“…In addition to experimentally verified GTPases [27], dynamin and clathrin, as well as sequences of several other key proteins have been detected in T. thermophila [10,156]. This includes several adaptor proteins (AP1, AP2, AP3) and coatomer (COP) subunits [157]. Furthermore, a collection of actin isoforms is part of the proteome inventory of ciliates [158].…”

Section: Signalling In Spines Of the Central Neurones-parallels With mentioning

confidence: 99%

The remembrance of the things past: Conserved signalling pathways link protozoa to mammalian nervous system

Plattner

Verkhratsky

2018

Cell Calcium

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The aim of the present article is to analyse the evolutionary links between protozoa and neuronal and neurosecretory cells. To this effect we employ functional and topological data available for ciliates, in particular for Paramecium. Of note, much less data are available for choanoflagellates, the progenitors of metazoans, which currently are in the focus of metazoan genomic data mining. Key molecular players are found from the base to the highest levels of eukaryote evolution, including neurones and neurosecretory cells. Several common fundamental mechanisms, such as SNARE proteins and assembly of exocytosis sites, GTPases, Ca-sensors, voltage-gated Ca-influx channels and their inhibition by the forming Ca/calmodulin complex are conserved, albeit with different subcellular channel localisation, from protozoans to man. Similarly, Ca-release channels represented by InsP receptors and putative precursors of ryanodine receptors, which all emerged in protozoa, serve for focal intracellular Ca signalling from ciliates to mammalian neuronal cells, eventually in conjunction with store-operated Ca-influx. Restriction of Ca signals by high capacity/low affinity Ca-binding proteins is maintained throughout the evolutionary tree although the proteins involved differ between the taxa. Phosphatase 2B/calcineurin appears to be involved in signalling and in membrane recycling throughout evolution. Most impressive example of evolutionary conservation is the sub-second dynamics of exocytosis-endocytosis coupling in Paramecium cells, with similar kinetics in neuronal and neurosecretory systems. Numerous cell surface receptors and channels that emerge in protozoa operate in the human nervous system, whereas a variety of cell adhesion molecules are newly "invented" during evolution, enabled by an increase in gene numbers, alternative splice forms and transcription factors. Thereby, important regulatory and signalling molecules are retained as a protozoan heritage.

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Conservation and Innovation in Tetrahymena Membrane Traffic: Proteins, Lipids, and Compartments

Cited by 23 publications

References 127 publications

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

An evolutionary balance: conservation vs innovation in ciliate membrane trafficking

Role of class III phosphatidylinositol 3-kinase during programmed nuclear death ofTetrahymena thermophila

The remembrance of the things past: Conserved signalling pathways link protozoa to mammalian nervous system

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