Basal Body Positioning Is Controlled by Flagellum Formation in Trypanosoma brucei

Absalon, Sabrina; Kohl, Linda; Branche, Carole; Blisnick, Thierry; Toutirais, Géraldine; Rusconi, Filippo; Cosson, Jacky; Bonhivers, Mélanie; Robinson, Derrick R.; Bastin, Philippe

doi:10.1371/journal.pone.0000437

Cited by 75 publications

(107 citation statements)

References 44 publications

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“…In the absence of IFT, the axoneme disassembles progressively from its distal end. The average length of the flagellum appears reduced in trypanosome IFT RNAi mutants (Absalon et al, 2008(Absalon et al, , 2007Kohl et al, 2003). However, the situation is complex because trypanosomes maintain their flagellum during the whole cell cycle.…”

Section: Ift Is Not Necessary For the Maintenance Of Flagellum Lengthmentioning

confidence: 99%

Intraflagellar transport is required for the maintenance of the trypanosome flagellum composition but not its length

Fort

Bonnefoy

Kohl

et al. 2016

Journal of Cell Science

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Intraflagellar transport (IFT) is required for construction of most cilia and flagella. Here, we used electron microscopy, immunofluorescence and live video microscopy to show that IFT is absent or arrested in the mature flagellum of Trypanosoma brucei upon RNA interference (RNAi)-mediated knockdown of IFT88 and IFT140, respectively. Flagella assembled prior to RNAi did not shorten, showing that IFT is not essential for the maintenance of flagella length. Although the ultrastructure of the axoneme was not visibly affected, flagellar beating was strongly reduced and the distribution of several flagellar components was drastically modified. The R subunit of the protein kinase A was no longer concentrated in the flagellum but was largely found in the cell body whereas the kinesin 9B motor was accumulating at the distal tip of the flagellum. In contrast, the distal tip protein FLAM8 was dispersed along the flagellum. This reveals that IFT also functions in maintaining the distribution of some flagellar proteins after construction of the organelle is completed.

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Section: Ift Is Not Necessary For the Maintenance Of Flagellum Lengthmentioning

confidence: 99%

Intraflagellar transport is required for the maintenance of the trypanosome flagellum composition but not its length

Fort

Bonnefoy

Kohl

et al. 2016

Journal of Cell Science

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“…These studies provided an important framework for considering the role of the cytoskeleton in mitochondrial genome segregation (Robinson and Gull, 1991;Robinson et al, 1995), though they did not directly implicate the flagellum as an active player in this process. Direct evidence for flagellum growth and flagellar beat in kinetoplast segregation has now come from RNAi studies in which several independent mutants with defective flagellum biogenesis or movement have a common defect in kinetoplast positioning (Dawe et al, 2005;Ralston et al, 2005Branche et al, 2006;Absalon et al, 2007b). At present it is still unclear precisely how the flagellum effects kinetoplast segregation, but a model (Absalon et al, 2007b) has been proposed in which the elongating new flagellum, which is tethered at the growing end by the flagellar connector (Moreira-Leite et al, 2001), exerts a reaction force on the basal body, driving movement of the new basal body/kinetoplast away from the old one (Absalon et al, 2007b).…”

Section: Cell Morphogenesismentioning

confidence: 99%

“…Direct evidence for flagellum growth and flagellar beat in kinetoplast segregation has now come from RNAi studies in which several independent mutants with defective flagellum biogenesis or movement have a common defect in kinetoplast positioning (Dawe et al, 2005;Ralston et al, 2005Branche et al, 2006;Absalon et al, 2007b). At present it is still unclear precisely how the flagellum effects kinetoplast segregation, but a model (Absalon et al, 2007b) has been proposed in which the elongating new flagellum, which is tethered at the growing end by the flagellar connector (Moreira-Leite et al, 2001), exerts a reaction force on the basal body, driving movement of the new basal body/kinetoplast away from the old one (Absalon et al, 2007b). Given the central importance of the flagellum and flagellar motility to trypanosome biology, it seems advantageous that segregation of the mitochondrial genome is linked to flagellum formation, maintenance and function.…”

Section: Cell Morphogenesismentioning

confidence: 99%

The flagellum of Trypanosoma brucei: New tricks from an old dog

Ralston

Hill

2008

International Journal for Parasitology

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African trypanosomes, i.e. Trypanosoma brucei and related sub-species, are devastating human and animal pathogens that cause significant human mortality and limit sustained economic development in sub-Saharan Africa. Trypanosoma brucei is a highly motile protozoan parasite and coordinated motility is central to both disease pathogenesis in the mammalian host and parasite development in the tsetse fly vector. Since motility is critical for parasite development and pathogenesis, understanding unique aspects of the T. brucei flagellum may uncover novel targets for therapeutic intervention in African sleeping sickness. Moreover, studies of conserved features of the T. brucei flagellum are directly relevant to understanding fundamental aspects of flagellum and cilium function in other eukaryotes, making T. brucei an important model system. The T. brucei flagellum contains a canonical 9 + 2 axoneme, together with additional features that are unique to kinetoplastids and a few closely-related organisms. Until recently, much of our knowledge of the structure and function of the trypanosome flagellum was based on analogy and inference from other organisms. There has been an explosion in functional studies in T. brucei in recent years, revealing conserved as well as novel and unexpected structural and functional features of the flagellum. Most notably, the flagellum has been found to be an essential organelle, with critical roles in parasite motility, morphogenesis, cell division and immune evasion. This review highlights recent discoveries on the T. brucei flagellum.

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“…In addition to mediating flagellum-cell body attachment, the FAZ filament also defines the cytokinesis cleavage plane (11,12), with the distal tip of the new FAZ filament marking the site of cytokinesis initiation (18 -20). Moreover, during the cell cycle in the procyclic form, the elongation of the FAZ filament positions the newly assembled basal body toward the cell posterior (21), which is crucial for organelle segregation and cell division (10,(22)(23)(24)(25).…”

mentioning

confidence: 99%

SAS-4 Protein in Trypanosoma brucei Controls Life Cycle Transitions by Modulating the Length of the Flagellum Attachment Zone Filament

Zhou

2015

Journal of Biological Chemistry

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The centrosome in animals constitutes the cell's microtubule-organizing center that nucleates spindle assembly, and is characterized by a symmetrical array of nine microtubule triplets emanating from a cartwheel structure in the very proximal region of the centriole. Biogenesis of centrioles requires many regulatory proteins, including SAS-6, SAS-4/CPAP, and BLD10/CEP135, which are thought to constitute the core ancestral module involved in centriole assembly (1). The three proteins have distinct functions in centriole biogenesis. SAS-6 assembles to the cartwheel (2, 3) and BLD10/CEP135 forms the pinhead that connects the cartwheel spokes to the A-microtubules of the microtubule triplets (4, 5), whereas SAS-4/CPAP controls the elongation of centriolar microtubules (6 -9).Trypanosoma brucei, a flagellated protozoan and the causative agent of human sleeping sickness, does not have centrosomes, but it possesses the basal body as its microtubule-organizing center to nucleate the assembly of a motile flagellum. The basal body is characterized by an array of nine microtubule triplets, with the conserved SAS-6 protein forming the cartwheel structure (10), similar to that of the centrosome in metazoa. The flagellum is attached, along most of its length, to the cell body via a specialized cytoskeletal structure termed the flagellum attachment zone (FAZ), 2 which consists of three main domains: the structure connecting the paraflagellar rod (PFR) to the flagellar membrane, the structure connecting the flagellar membrane and the cell body membrane, and a cytoplasmic filament (often referred to as the FAZ filament) and its associated microtubule quartet (11)(12)(13)(14)(15)(16)(17). In addition to mediating flagellum-cell body attachment, the FAZ filament also defines the cytokinesis cleavage plane (11,12), with the distal tip of the new FAZ filament marking the site of cytokinesis initiation (18 -20). Moreover, during the cell cycle in the procyclic form, the elongation of the FAZ filament positions the newly assembled basal body toward the cell posterior (21), which is crucial for organelle segregation and cell division (10,(22)(23)(24)(25).Trypanosomatids, a group of kinetoplastid parasites consisting of T. brucei, Trypanosoma cruzi, and Leishmania spp., appear in a variety of different morphological forms during their life cycle and are distinguished by the relative position of the kinetoplast (mitochondrial DNA) and the nucleus and by the position, length, and cell body attachment of the flagellum (26). In the tsetse fly vector, T. brucei differentiates from the trypomastigote form to the epimastigote form, which undergoes asymmetrical cell division to produce a long epimastigote cell and a short epimastigote cell (26). How life cycle transitions in T. brucei are regulated is largely unknown, but recent work has begun to uncover the regulators involved in this process. ALBA3 and ALBA4, two closed related RNA-binding proteins, are the first factors found to be involved in life cycle transitions in T. brucei (27). Anothe...

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Basal Body Positioning Is Controlled by Flagellum Formation in Trypanosoma brucei

Cited by 75 publications

References 44 publications

Intraflagellar transport is required for the maintenance of the trypanosome flagellum composition but not its length

Intraflagellar transport is required for the maintenance of the trypanosome flagellum composition but not its length

The flagellum of Trypanosoma brucei: New tricks from an old dog

SAS-4 Protein in Trypanosoma brucei Controls Life Cycle Transitions by Modulating the Length of the Flagellum Attachment Zone Filament

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