Tubulin polyglutamylation regulates flagellar motility by controlling a specific inner‐arm dynein that interacts with the dynein regulatory complex

Kubo, Tomohiro; Yagi, Toshiki; Kamiya, Ritsu

doi:10.1002/cm.21075

Cited by 47 publications

(50 citation statements)

References 52 publications

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“…Ttll9 deficiency strongly affected the beating pattern of murine sperm flagella, in contrast with the Chlamydomonas mutant lacking functional TTLL9, which shows an almost normal beating pattern (Kubo et al, 2010(Kubo et al, , 2012. We often observed active beats of Ttll9 −/− spermatozoa at distal flagellum that showed a stall at the proximal region (Movie 2).…”

Section: Discussionmentioning

confidence: 91%

“…The importance of the PTMs of motile flagella and cilia has been reported previously in various models, such as mouse (Ikegami et al, 2010;Lee et al, 2013), ependymal cells (Bosch Grau et al, 2013), Tetrahymena Suryavanshi et al, 2010) and Chlamydomonas (Kubo et al, 2010(Kubo et al, , 2012. Recently, a few reports on transgenic mouse models have also underlined the importance of polyglutamylation in spermatozoa.…”

Section: Introductionmentioning

confidence: 80%

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Ttll9 −/− mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating

Konno

Ikegami

Konishi

et al. 2016

Journal of Cell Science

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Nine outer doublet microtubules in axonemes of flagella and cilia are heterogeneous in structure and biochemical properties. In mammalian sperm flagella, one of the factors to generate the heterogeneity is tubulin polyglutamylation, although the importance of the heterogeneous modification is unclear. Here, we show that a tubulin polyglutamylase Ttll9 deficiency (Ttll9) causes a unique set of phenotypes related to doublet heterogeneity. Ttll9 −/− sperm axonemes had frequent loss of a doublet and reduced polyglutamylation. Intriguingly, the doublet loss selectively occurred at the distal region of doublet 7, and reduced polyglutamylation was observed preferentially on doublet 5. Ttll9 −/− spermatozoa showed aberrant flagellar beating, characterized by frequent stalls after antihook bending. This abnormal motility could be attributed to the reduction of polyglutamylation on doublet 5, which probably occurred at a position involved in the switching of bending. These results indicate that mammalian Ttll9 plays essential roles in maintaining the normal structure and beating pattern of sperm flagella by establishing normal heterogeneous polyglutamylation patterns.

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Section: Discussionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 80%

Ttll9 −/− mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating

Konno

Ikegami

Konishi

et al. 2016

Journal of Cell Science

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“…The B-tubule is characterized by a content of posttranslationally modified tubulin higher than the A-tubule and, in Chlamydomonas, glutamylated tubulin is preferentially localized in the B-tubule (Kubo et al, 2010). A regulatory role for tubulin posttranslational modifications has been demonstrated for the interaction between motors and microtubules (Kubo et al, 2010(Kubo et al, , 2012Suryavanshi et al, 2010), and might be expected to act on IFT motors as well.…”

Section: Discussion Short Ift Trains Are Involved In Anterograde Tranmentioning

confidence: 99%

Two classes of short intraflagellar transport train with different 3D structures are present in Chlamydomonas flagella

Vannuccini

Paccagnini

Cantele

et al. 2016

Journal of Cell Science

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Intraflagellar transport (IFT) is responsible for the bidirectional trafficking of molecular components required for the elongation and maintenance of eukaryotic cilia and flagella. Cargo is transported by IFT 'trains', linear rows of multiprotein particles moved by molecular motors along the axonemal doublets. We have previously described two structurally distinct categories of 'long' and 'short' trains. Here, we analyse the relative number of these trains throughout flagellar regeneration and show that long trains are most abundant at the beginning of flagellar growth whereas short trains gradually increase in number as flagella elongate. These observations are incompatible with the previous hypothesis that short trains are derived solely from the reorganization of long trains at the flagellar tip. We demonstrate with electron tomography the existence of two distinct ultrastructural organizations for the short trains, we name these 'narrow' and 'wide', and provide the first 3D model of the narrow short trains. These trains are characterized by tri-lobed units, which repeat longitudinally every 16 nm and contact protofilament 7 of the B-tubule. Functional implications of the new structural evidence are discussed.

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“…Taken together, these observations suggest that the I1 complex may act more as a mobile spacer than as a source of torque generation. Kubo et al (2012) found that dynein e, which is also heavily associated with the drc/nexin, also plays a peculiar role in motility regulation. It binds more strongly to polyglutamylated tubulin, which improves the active beating of the flagellum, yet it actually slows down the rate at which the doublets disintegrate by sliding.…”

Section: Strange Flagella Mutant Flagella and Frayed Flagellamentioning

confidence: 99%

The geometric clutch at 20: stripping gears or gaining traction?

Lindemann

Lesich

2015

Reproduction

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It has been 20 years since the geometric clutch (GC) hypothesis was first proposed. The core principle of the GC mechanism is fairly simple. When the axoneme of a eukaryotic flagellum is bent, mechanical stress generates forces transverse to the outer doublets (t-forces). These t-forces can push doublets closer together or pry them apart. The GC hypothesis asserts that changes in the inter-doublet spacing caused by t-forces are responsible for the activation and deactivation of the dynein motors, that creates the beat cycle. A series of computer models utilizing the clutch mechanism has shown that it can simulate ciliary and flagellar beating. The objective of the present review is to assess where things stand with the GC hypothesis in the clarifying light of new information. There is considerable new evidence to support the hypothesis. However, it is also clear that it is necessary to modify some of the original conceptions of the hypothesis so that it can be consistent with the results of recent experimental and ultrastructural studies. In particular, dynein deactivation by t-forces must be able to occur with dyneins that remain attached to the B-subtubule of the adjacent doublet.Reproduction (2015) 150 R45-R53

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Tubulin polyglutamylation regulates flagellar motility by controlling a specific inner‐arm dynein that interacts with the dynein regulatory complex

Cited by 47 publications

References 52 publications

Ttll9 −/− mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating

Ttll9 −/− mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating

Two classes of short intraflagellar transport train with different 3D structures are present in Chlamydomonas flagella

The geometric clutch at 20: stripping gears or gaining traction?

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