Modes of flagellar assembly in Chlamydomonas reinhardtii and Trypanosoma brucei

Höög, Johanna L.; Lacomble, Sylvain; O’Toole, Eileen; Hoenger, Andreas; McIntosh, J. Richard; Gull, Keith

doi:10.7554/elife.01479

Cited by 68 publications

(65 citation statements)

References 64 publications

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“…A similar variability in MT termination patterns was also described for rodent sperm after conventional fixation . In addition, plunge‐frozen T. brucei flagella showed comparable tip ultrastructures to high‐pressure frozen or chemically fixed samples , suggesting that flagellar MT termination patterns are not noticeably disturbed during cryo‐EM preparation.…”

Section: Discussionsupporting

confidence: 68%

“…S1), unlike in C. reinhardtii , and a long singlet region is present (Fig. A‐F), unlike in T. brucei .…”

Section: Discussionmentioning

confidence: 96%

“…In the flagellar tips of model organisms like Chlamydomonas reinhardtii or Tetrahymena thermophila , the incomplete B‐tubules of dMTs end and the A‐tubules extend together with the CP to the tip extremity, creating the singlet region . However, this region is completely absent in other models like Leishmania mexicana and Trypanosoma brucei . In rodent spermatozoa, the singlet region includes the CP together with pairs of ‘duplex’ MTs – singlet MTs (sMT) extensions of A‐ and B‐tubules from the same dMT .…”

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confidence: 99%

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Axonemal doublet microtubules can split into two complete singlets in human sperm flagellum tips

2019

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Motile flagella are crucial for human fertility and embryonic development. The distal tip of the flagellum is where growth and intra‐flagellar transport are coordinated. In most model organisms, but not all, the distal tip includes a ‘singlet region’, where axonemal doublet microtubules (dMT) terminate and only complete A‐tubules extend as singlet microtubules (sMT) to the tip. How a human flagellar tip is structured is unknown. Here, the flagellar tip structure of human spermatozoa was investigated by cryo‐electron tomography, revealing the formation of a complete sMT from both the A‐tubule and B‐tubule of dMTs. This different tip arrangement in human spermatozoa shows the need to investigate human flagella directly in order to understand their role in health and disease.

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Section: Discussionsupporting

confidence: 68%

“…S1), unlike in C. reinhardtii , and a long singlet region is present (Fig. A‐F), unlike in T. brucei .…”

Section: Discussionmentioning

confidence: 96%

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confidence: 99%

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Axonemal doublet microtubules can split into two complete singlets in human sperm flagellum tips

2019

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“…S10), so the kinesin is likely capable of active motility. The force exerted by the kinesin on the microtubule ends, together with the lack of various axonemal complexes in this part of the axoneme, may explain the microtubule disorganization observed in the distal axonemal region of a growing T. brucei flagellum (33). In plants, kinesin-15s were shown to attach plus ends of dynamic microtubules to the middle region of the phragmoplast, the key structure for plant cytokinesis (34).…”

Section: The Fc Is a Membrane Junction Attached By Two Types Of Kinesmentioning

confidence: 99%

Protein diversity in discrete structures at the distal tip of the trypanosome flagellum

Varga

Moreira-Leite

Portman

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The distal end of the eukaryotic flagellum/cilium is important for axonemal growth and signaling and has distinct biomechanical properties. Specific flagellum tip structures exist, yet their composition, dynamics, and functions are largely unknown. We used biochemical approaches to identify seven constituents of the flagella connector at the tip of an assembling trypanosome flagellum and three constituents of the axonemal capping structure at the tips of both assembling and mature flagella. Both tip structures contain evolutionarily conserved as well as kinetoplastid-specific proteins, and component assembly into the structures occurs very early during flagellum extension. Localization and functional studies reveal that the flagella connector membrane junction is attached to the tips of extending microtubules of the assembling flagellum by a kinesin-15 family member. On the opposite side, a kinetoplastid-specific kinesin facilitates attachment of the junction to the microtubules in the mature flagellum. Functional studies also suggest roles of several other components and the definition of subdomains in the tip structures.

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“…The basal plate anchors at least one microtubule of the central pair (18,19) and is derived from two electron-dense discs that cross the distal TZ (20).…”

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confidence: 99%

Cilium transition zone proteome reveals compartmentalization and differential dynamics of ciliopathy complexes

Dean

Moreira-Leite

Varga

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The transition zone (TZ) of eukaryotic cilia and flagella is a structural intermediate between the basal body and the axoneme that regulates ciliary traffic. Mutations in genes encoding TZ proteins (TZPs) cause human inherited diseases (ciliopathies). Here, we use the trypanosome to identify TZ components and localize them to TZ subdomains, showing that the Bardet-Biedl syndrome complex (BBSome) is more distal in the TZ than the Meckel syndrome (MKS) complex. Several of the TZPs identified here have human orthologs. Functional analysis shows essential roles for TZPs in motility, in building the axoneme central pair apparatus and in flagellum biogenesis. Analysis using RNAi and HaloTag fusion protein approaches reveals that most TZPs (including the MKS ciliopathy complex) show long-term stable association with the TZ, whereas the BBSome is dynamic. We propose that some Bardet-Biedl syndrome and MKS pleiotropy may be caused by mutations that impact TZP complex dynamics.transition zone | cilium/flagellum | BBSome | MKS/B9 complex | trypanosome C ilia, or flagella (the two terms are used here interchangeably), are multifunctional organelles that were present in the last common eukaryotic ancestor (1). Defects in cilia are responsible for pleiotropic human diseases (called ciliopathies) and their function is essential for pathogenesis in protozoan parasites (2, 3).During ciliogenesis, a microtubule organizing center called the "basal body" docks at the membrane. Basal bodies are built from nine microtubule triplets and two microtubules from each triplet extend to form a transition zone (TZ) and, ultimately, the axoneme. Thus, the TZ represents a structural junction between the basal body and the axoneme.As expected from its strategic position between the basal body and the axoneme, the TZ acts as a "ciliary gate" that controls ciliary composition and function (4). Many ciliopathies are caused by defects in complexes that associate with the TZ, including Meckel syndrome (MKS), Joubert syndrome and Bardet-Biedl syndrome (BBS). Studies using murine kidney epithelial cells and embryos suggest that the MKS complex demarcates the ciliary membrane by forming a diffusion barrier at the base of the cilium (5-7). On the other hand, the BBS complex (BBSome) is an adapter for intraflagellar transport (IFT) complexes that cross the TZ barrier to transport sensory proteins between the ciliary membrane and the cell body (8, 9).The TZ has distinctive structural features. At the proximal boundary of the TZ, where the basal body C tubule terminates, a "terminal plate" crosses the TZ. Studies in Tetrahymena suggest that the terminal plate contains pores for the passage of IFT "trains" that deliver axonemal components to the distal tip of flagella (10). Striated transitional fibers radiate from the distal end of the basal body triplets to join the plasma membrane (11-14), forming blades thought to create a physical barrier preventing vesicles from entering the ciliary lumen. Electron microscopy (EM) studies in Chlamydomonas suggest that...

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Modes of flagellar assembly in Chlamydomonas reinhardtii and Trypanosoma brucei

Cited by 68 publications

References 64 publications

Axonemal doublet microtubules can split into two complete singlets in human sperm flagellum tips

Axonemal doublet microtubules can split into two complete singlets in human sperm flagellum tips

Protein diversity in discrete structures at the distal tip of the trypanosome flagellum

Cilium transition zone proteome reveals compartmentalization and differential dynamics of ciliopathy complexes

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