The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding

F. D. Warner, P. Satir

Research output: Contribution to journalArticle

208 Citations (Scopus)

Abstract

The sliding microtubule model of ciliary motility predicts that cumulative local displacement (Δl) of doublet microtubules relative to one another occurs only in bent regions of the axoneme. This prediction was tested by using the radial spokes which join the A subfiber of each doublet to the central sheath as markers of microtubule alignment to measure sliding displacements directly. Gill cilia from the mussel E. complanatus have radial spokes lying in groups of 3 which repeat at 860 Å along the A subfiber. The spokes are aligned with the 2 rows of projections along each of the central microtubules that form the central sheath. The projections repeat at 143 Å and form a vernier with the radial spokes in the precise ratio of 6 projection repeats to 1 spoke group repeat. In straight regions of the axoneme, either proximal or distal to a bend, the relative position of spoke groups between any 2 doublets remains constant for the length of that region. However, in bent regions, the position of spoke groups changes systematically so that Δl (doublet 1 vs. 5) can be seen to accumulate at a maximum of 122 Å per successive 860 Å spoke repeat. Local contraction of microtubules is absent. In straight regions of the axoneme, the radial spokes lie in either of 2 basic configurations: the parallel configuration where spokes 1-3 of each group are normal (90°) to subfiber A, and the tilted spoke 3 configuration where spoke 3 forms an angle of 9-20°. Since considerable sliding of doublets relative to the central sheath (650 Å) has usually occurred in these regions, the spokes must be considered, functionally, as detached from the sheath projections. In bent regions of the axoneme, 2 additional spoke configurations occur where all 3 spokes of each group are tilted to a maximum of ± 33° from normal. Since the spoke angles do not lie on radii through the center of bend curvature, and Δl accumulates in the bend, the spokes must be considered as attached to the sheath when bending occurs. The observed radial spoke configurations strongly imply that there is a precise cycle of spoke detachment reattachment to the central sheath which it is concluded forms the main part of the mechanism converting active interdoublet sliding into local bending.

Original languageEnglish (US)
Pages (from-to)35-63
Number of pages29
JournalJournal of Cell Biology
Volume63
Issue number1
StatePublished - 1974
Externally publishedYes

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Axoneme
Microtubules
Cilia
Bivalvia

ASJC Scopus subject areas

  • Cell Biology

Cite this

The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. / Warner, F. D.; Satir, P.

In: Journal of Cell Biology, Vol. 63, No. 1, 1974, p. 35-63.

Research output: Contribution to journalArticle

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abstract = "The sliding microtubule model of ciliary motility predicts that cumulative local displacement (Δl) of doublet microtubules relative to one another occurs only in bent regions of the axoneme. This prediction was tested by using the radial spokes which join the A subfiber of each doublet to the central sheath as markers of microtubule alignment to measure sliding displacements directly. Gill cilia from the mussel E. complanatus have radial spokes lying in groups of 3 which repeat at 860 {\AA} along the A subfiber. The spokes are aligned with the 2 rows of projections along each of the central microtubules that form the central sheath. The projections repeat at 143 {\AA} and form a vernier with the radial spokes in the precise ratio of 6 projection repeats to 1 spoke group repeat. In straight regions of the axoneme, either proximal or distal to a bend, the relative position of spoke groups between any 2 doublets remains constant for the length of that region. However, in bent regions, the position of spoke groups changes systematically so that Δl (doublet 1 vs. 5) can be seen to accumulate at a maximum of 122 {\AA} per successive 860 {\AA} spoke repeat. Local contraction of microtubules is absent. In straight regions of the axoneme, the radial spokes lie in either of 2 basic configurations: the parallel configuration where spokes 1-3 of each group are normal (90°) to subfiber A, and the tilted spoke 3 configuration where spoke 3 forms an angle of 9-20°. Since considerable sliding of doublets relative to the central sheath (650 {\AA}) has usually occurred in these regions, the spokes must be considered, functionally, as detached from the sheath projections. In bent regions of the axoneme, 2 additional spoke configurations occur where all 3 spokes of each group are tilted to a maximum of ± 33° from normal. Since the spoke angles do not lie on radii through the center of bend curvature, and Δl accumulates in the bend, the spokes must be considered as attached to the sheath when bending occurs. The observed radial spoke configurations strongly imply that there is a precise cycle of spoke detachment reattachment to the central sheath which it is concluded forms the main part of the mechanism converting active interdoublet sliding into local bending.",
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