The radial spokes and central apparatus: Mechano‐chemical transducers that regulate flagellar motility

Smith, Elizabeth F.; Yang, Pinfen

doi:10.1002/cm.10155

Cited by 268 publications

(276 citation statements)

References 108 publications

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“…The notion that the CPC and the radial spokes are important for the regulation of the flagellar waveform is not new (7,35). Our data, however, inform this debate by showing a correlation between bilateral symmetry of the internal flagellar structures and the waveform of sea urchin sperm flagella.…”

Section: Discussionmentioning

confidence: 50%

“…Differences in the macromolecular composition and in spatial arrangement of axoneme components (e.g., the absence of an S3 radial spoke and the rotating CPC in Chlamydomonas) (26) coincide nicely with the fundamentally different waveforms of these flagella. Although the radial spoke system and CPC are not essential for axonemal motility per se, their interactions may be important for controlling the size and shape of the waveforms that can be altered in response to specific stimuli (35,40). For instance, the symmetry of axonemal bends is often modified by changes in the calcium concentration of the surrounding medium (44).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography

Nicastro

McIntosh

Baumeister

2005

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

158

121

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We have used cryo-electron tomography to investigate the 3D structure and macromolecular organization of intact, frozenhydrated sea urchin sperm flagella in a quiescent state. The tomographic reconstructions provide information at a resolution better than 6 nm about the in situ arrangements of macromolecules that are key for flagellar motility. We have visualized the heptameric rings of the motor domains in the outer dynein arm complex and determined that they lie parallel to the plane that contains the axes of neighboring flagellar microtubules. Both the material associated with the central pair of microtubules and the radial spokes display a plane of symmetry that helps to explain the planar beat pattern of these flagella. Cryo-electron tomography has proven to be a powerful technique for helping us understand the relationships between flagellar structure and function and the design of macromolecular machines in situ.axoneme ͉ dynein ͉ microtubule ͉ motility ͉ sperm E ukaryotic cilia and flagella are highly ordered organelles that are used by a great variety of species and cell types to generate motion. Despite the diversity of their motile functions, the basic architecture of these machines is remarkably conserved (for review, see ref. 1). All such structures are built on an ordered assembly of microtubules known as the axoneme. The most widely distributed form of the axoneme consists of nine outer microtubule doublets (MTDs) and two singlet microtubules (2, 3). The combination of many structural and enzymatic studies with in vitro motility assays and computer-based simulations has laid a framework for our understanding about how flagellar motion is generated. Sliding between pairs of outer MTDs is powered by the dynein ATPases and converted into flagellar bending as a result of constraints imposed on interdoublet sliding by protein cross-links, such as nexin, which lie between adjacent MTDs (for reviews, see refs. 4 and 5). For an axoneme to generate the complex motions typical of beating cilia and flagella, there must be precise control of dynein's action, both around the circumference and along the length of the axoneme.Because of their biological and medical importance and their utility as a model for other forms of microtubule-based motility (6), flagella and cilia have been studied extensively (for reviews, see refs. 3, 5, and 7-9). However, despite the increase in knowledge about isolated components of the axoneme, much remains to be learned about the mechanical and regulatory mechanisms underlying flagellar motion (3, 10). To elucidate the role of all of the players in axoneme motility, one will need a better understanding of the organization of axonemal elements in situ at a resolution that will characterize the structural changes that they undergo during functional cycles.Sea urchin sperm tails are an admirable material for this sort of study because they are built with a classic ''9 ϩ 2'' axoneme, and their beat pattern is mainly planar, greatly simplifying the geometry of their function in compari...

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Section: Discussionmentioning

confidence: 50%

Section: Discussionmentioning

confidence: 99%

3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography

Nicastro

McIntosh

Baumeister

2005

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

158

121

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“…Correlations between rotation of central pair microtubules and switching have been described [Omoto et al, 1999;Mitchell, 2003]. There is also extensive biochemical evidence that dynein activity, measured by sliding disintegration assays, can be regulated by components of the central apparatus [Smith and Yang, 2004]. Together, these observations indicate a role for the central apparatus in production of specific bending patterns.…”

Section: If There Are On and Off Modes Of Dynein There Must Be A Switchmentioning

confidence: 91%

Thinking about flagellar oscillation

Brokaw

2008

Cell Motil. Cytoskeleton

138

133

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Bending of cilia and flagella results from sliding between the microtubular outer doublets, driven by dynein motor enzymes. This review reminds us that many questions remain to be answered before we can understand how dynein-driven sliding causes the oscillatory bending of cilia and flagella. Does oscillation require switching between two distinct, persistent modes of dynein activity? Only one mode, an active forward mode, has been characterized, but an alternative mode, either inactive or reverse, appears to be required. Does switching between modes use information from curvature, sliding direction, or both? Is there a mechanism for reciprocal inhibition? Can a localized capability for oscillatory sliding become self-organized to produce the metachronal phase differences required for bend propagation? Are interactions between adjacent dyneins important for regulation of oscillation and bend propagation? Cell Motil. Cytoskeleton 66: 425-436, 2009. '

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“…This differs from Chlamydomonas reinhardtii, a well-established model system for flagellum studies, where the central pair rotates within the axoneme (Omoto et al, 1999;Mitchell, 2003). Rotation of the asymmetrically arranged central pair apparatus in C. reinhardtii has been hypothesized to play a role in activating distinct sets of dyneins on the outer doublets (Wargo and Smith, 2003;Smith and Yang, 2004). Thus, a non-rotating central pair in T. brucei may reflect or impose unique demands on dynein motor regulation.…”

Section: Axonemementioning

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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The radial spokes and central apparatus: Mechano‐chemical transducers that regulate flagellar motility

Cited by 268 publications

References 108 publications

3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography

3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography

Thinking about flagellar oscillation

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

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