Flagellar incorporation of proteins follows at least two different routes in trypanosomes

Vincensini, Laetitia; Blisnick, Thierry; Bertiaux, Éloïse; Hutchinson, Sebastian; Georgikou, Christina; Ooi, Cher-Pheng; Bastin, Philippe

doi:10.1111/boc.201700052

Cited by 10 publications

(7 citation statements)

References 81 publications

(130 reference statements)

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“…Here, we selected the protist Trypanosoma brucei for investigation for several reasons. First, its axoneme is very stable [11] and relies on IFT for construction [12,13] but not for length maintenance [14], exactly like in spermatozoa or photoreceptors. IFT remains active after assembly to maintain other elements but not axoneme composition [14].…”

Section: Introductionmentioning

confidence: 99%

A Grow-and-Lock Model for the Control of Flagellum Length in Trypanosomes

et al. 2018

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Highlights d The total amount of IFT material increases linearly during flagellum elongation d Reducing IFT rate by knocking down IFT kinesin motors slows down the growth rate d Increasing IFT rate in a locked flagellum does not lead to further elongation d The locking event is initiated prior to cell division SUMMARY Several models have been proposed to explain how eukaryotic cells control the length of their cilia and flagella.Here, we investigated this process in the protist Trypanosoma brucei, an excellent model system for cells with stable cilia like photoreceptors or spermatozoa. We show that the total amount of intraflagellar transport material (IFT, the machinery responsible for flagellum construction) increases during flagellum elongation, consistent with constant delivery of precursors and the previously reported linear growth. Reducing the IFT frequency by RNAi knockdown of the IFT kinesin motors slows down the elongation rate and results in the assembly of shorter flagella. These keep on elongating after cell division but fail to reach the normal length. This failure is neither due to an absence of precursors nor to a morphogenetic control by the cell body. We propose that the flagellum is locked after cell division, preventing further elongation or shortening. This is supported by the fact that subsequent increase in the IFT rate does not lead to further elongation. The distal tip FLAM8 protein was identified as a marker for the locking event. It is initiated prior to cell division, leading to an arrest of elongation in the daughter cell. Here, we propose a new model termed ''grow and lock'' where the flagellum elongates until a locking event takes place in a timely defined manner, hence fixing length. Alteration in the growth rate and/ or in the timing of the locking event would lead to the formation of flagella of different lengths.

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Section: Introductionmentioning

confidence: 99%

A Grow-and-Lock Model for the Control of Flagellum Length in Trypanosomes

et al. 2018

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“…A second involves membraneassociated transport, in which proteins move from the cell membrane to the flagellar membrane (Vincensini et al, 2018). The flagellar arginine kinase of Trypanosoma brucei, AK3, is membrane-associated and delivered to flagella independently of IFT (Vincensini et al, 2018). In non-oomycetes, some PKs have been shown to be anchored to membranes by lipidation (Michibata et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Phosphagen kinase function in flagellated spores of the oomycete Phytophthora infestans integrates transcriptional regulation, metabolic dynamics and protein retargeting

Kagda

Ah‐Fong

et al. 2018

Molecular Microbiology

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Flagellated spores play important roles in the infection of plants and animals by many eukaryotic microbes. The oomycete Phytophthora infestans, which causes potato blight, expresses two phosphagen kinases (PKs). These enzymes store energy in taurocyamine, and are hypothesized to resolve spatial and temporal imbalances between rates of ATP creation and use in zoospores. A dimeric PK is found at low levels in vegetative mycelia, but high levels in ungerminated sporangia and zoospores. In contrast, a monomeric PK protein is at similar levels in all tissues, although is transcribed primarily in mycelia. Subcellular localization studies indicate that the monomeric PK is mitochondrial. In contrast, the dimeric PK is cytoplasmic in mycelia and sporangia but is retargeted to flagellar axonemes during zoosporogenesis. This supports a model in which PKs shuttle energy from mitochondria to and through flagella. Metabolite analysis indicates that deployment of the flagellar PK is coordinated with a large increase in taurocyamine, synthesized by sporulation-induced enzymes that were lost during the evolution of zoospore-lacking oomycetes. Thus, PK function is enabled by coordination of the transcriptional, metabolic and protein targeting machinery during the life cycle. Since plants lack PKs, the enzymes may be useful targets for inhibitors of oomycete plant pathogens.

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“…For example, structural proteins composing the T. brucei axoneme or the associated paraflagellar rod are very stable after assembly, whereas the membrane-associated arginine kinase shows a rapid turnover in both elongating and nongrowing flagella (Bastin et al, 1999;Vincensini et al, 2018). If tubulin access is restricted in the mature flagellum, it should nevertheless be sufficient to maintain axoneme length in case microtubules depolymerise.…”

Section: Cells With Two Temporally Distinct Flagella: Age Discriminmentioning

confidence: 99%

“…Here, the cell faces a situation where one flagellum elongates and requires a lot of new precursors, whereas the length of the mature one remains unchanged (Sherwin & Gull, 1989a). At least in Trypanosoma brucei, various experiments showed that there is little turnover of structural components in the mature flagellum (Bastin, MacRae, Francis, Matthews, & Gull, 1999;Fort, Bonnefoy, Kohl, & Bastin, 2016;Vincensini et al, 2018). How does the cell proceed to elongate only the new flagellum?…”

Section: Cells With Two Temporally Distinct Flagella: Age Discriminmentioning

confidence: 99%

“…We should also not forget that flagella contain very different types of proteins whose behaviour could vary significantly; hence, models could be relevant for some types of proteins only. For example, structural proteins composing the T. brucei axoneme or the associated paraflagellar rod are very stable after assembly, whereas the membrane-associated arginine kinase shows a rapid turnover in both elongating and nongrowing flagella (Bastin et al, 1999;Vincensini et al, 2018).…”

Section: Cells With Two Temporally Distinct Flagella: Age Discriminmentioning

confidence: 99%

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Dealing with several flagella in the same cell

Bertiaux

Bastin

2020

Cellular Microbiology

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Flagella are sophisticated organelles found in many eukaryotic microbes where they perform functions related to motility, signal detection, or cell morphogenesis. In many cases, several flagella are present per cell, and these can have a different composition, length, age, or function, raising the question of how this is managed. When the flagella are equivalent and constructed simultaneously such as in Chlamydomonas or Naegleria, we propose an equal access model where molecular components have free access to each organelle. By contrast, Trypanosoma and Leishmania contain temporally distinct organelles and elongate a new flagellum whilst maintaining the existing one. The equal access model could function providing that the mature flagellum is "locked" so that it can no longer be elongated or shortened. Alternatively, access of flagellar components could be restricted at the level of the basal body, the transition zone, or the loading on intraflagellar transport trains. In organisms that contains flagella of different age and composition such as Giardia, a temporal dimension is necessary, with the production of protein components of flagella spreading over one or more cell cycles. In the future, deciphering the molecular mechanisms involved in these processes should reveal new insights in flagellum assembly and function.

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Flagellar incorporation of proteins follows at least two different routes in trypanosomes

Cited by 10 publications

References 81 publications

A Grow-and-Lock Model for the Control of Flagellum Length in Trypanosomes

A Grow-and-Lock Model for the Control of Flagellum Length in Trypanosomes

Phosphagen kinase function in flagellated spores of the oomycete Phytophthora infestans integrates transcriptional regulation, metabolic dynamics and protein retargeting

Dealing with several flagella in the same cell

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