Dynein arm attachment probed with a non-hydrolyzable ATP analog. Structural evidence for patterns of activity

Bennet Spungin, Jock Avolio, Stuart Arden, Peter Satir

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

The dynein arms that power ciliary motility are normally permanently attached by one end exclusively to subfiber A of each axonemal doublet (N) while the other (head) end transiently attaches to the subfiber B of the adjacent doublet (N + 1) to produce sliding of the doublets. In Tetrahymena axonemes, sliding of contiguous groups of doublets is induced by ATP suggesting that, in the absence of exogenous protease, there may be sets of potentially active and potentially inactive or refractory arms in a single axoneme. In the presence of a non-hydrolyzable analog of ATP, β,γ-methylene adenosine 5′-triphosphate (AMP-PCP), about half the doublets in an axonemal preparation retain all arms bound to subfiber A, but half the doublets show long regions where some arms are pulled away from subfiber A of doublet N and attached to subfiber B of doublet N + 1 by their head ends. In AMP-PCP-induced splaying, positional information regarding arm state is retained. Analysis reveals that throughout regions where B subfiber attachment is found, small groups of about four subfiber B attached arms alternate with groups of about four arms that remain attached to subfiber A. This unique pattern of attachment suggests that arms function co-operatively in groups of four. Further, the repetition of the pattern is reminiscent of metachronal activity seen at higher levels of biological organization. This suggests that in these regions we have instantaneously preserved groups of arms capable of attaching to and detaching from doublet N + 1 in rapid succession. This appearance could be used to delineate the potentially active sets of arm, primed for mechanochemical activity, within an axoneme.

Original languageEnglish (US)
Pages (from-to)671-677
Number of pages7
JournalJournal of Molecular Biology
Volume197
Issue number4
DOIs
StatePublished - Oct 20 1987

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Dyneins
Arm
Adenosine Triphosphate
Axoneme
Head
Tetrahymena
Peptide Hydrolases

ASJC Scopus subject areas

  • Virology

Cite this

Dynein arm attachment probed with a non-hydrolyzable ATP analog. Structural evidence for patterns of activity. / Spungin, Bennet; Avolio, Jock; Arden, Stuart; Satir, Peter.

In: Journal of Molecular Biology, Vol. 197, No. 4, 20.10.1987, p. 671-677.

Research output: Contribution to journalArticle

Spungin, Bennet ; Avolio, Jock ; Arden, Stuart ; Satir, Peter. / Dynein arm attachment probed with a non-hydrolyzable ATP analog. Structural evidence for patterns of activity. In: Journal of Molecular Biology. 1987 ; Vol. 197, No. 4. pp. 671-677.
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