DC3, the Smallest Subunit of the Chlamydomonas Flagellar Outer Dynein Arm-docking Complex, Is a Redox-sensitive Calcium-binding Protein

Casey, Diane M.; Yagi, Toshiki; Kamiya, Ritsu; Witman, George B.

doi:10.1074/jbc.m303064200

Cited by 44 publications

(42 citation statements)

References 47 publications

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“…Their flagella lack the outer dynein arms and beat with roughly one-half wild-type frequency. However, oda1 also lacks the outer dynein arm docking complex proteins, which include a potential Ca 2+ sensor (Casey et al, 2003a;Casey et al, 2003b). The results of all analyses for all strains and conditions tested are presented in tabular form in Table 2.…”

Section: Resultsmentioning

confidence: 99%

“…Interestingly, we have previously shown that the C1 microtubule of the central apparatus is not oriented towards the region of active sliding in either pf28 or oda1 axonemes, indicating that in the absence of the outer dynein arms, regulatory cues produced by the central apparatus are uncoupled from microtubule sliding under high Ca 2+ conditions (Wargo and Smith, 2003). While pf28 axonemes lack the outer dynein arms, which is the same defect as in oda1, oda1 axonemes additionally lack the outer dynein arm docking complex, which includes DC3, a Ca 2+ sensitive binding protein (Casey et al, 2003a;Casey et al, 2003b). These results suggest a possible role for DC3 in modulating dynein-driven microtubule sliding in response to increases in Ca 2+ .…”

Section: Sliding Pattern Correlates With Waveformmentioning

confidence: 93%

“…However, previous studies in Chlamydomonas suggest that the effect is mediated in part by calmodulin associated with the axoneme (Smith, 2002a;Yang et al, 2001). Additional Ca 2+ binding proteins that may play a role in Ca 2+ induced changes in motility include the Ca 2+ binding protein centrin/caltractin (Guerra et al, 2003;Huang et al, 1988;Piperno et al, 1992;Salisbury et al, 1988;Yanagisawa and Kamiya, 2001), the 18 kDa light chain of the outer dynein arm in Chlamydomonas (King and Patel-King, 1995), a Ca 2+ regulated nucleotide-diphosphate kinase in Chlamydomonas flagella (Patel-King et al, 2002) and the outer dynein arm docking complex protein DC3 (Casey et al, 2003a;Casey et al, 2003b). …”

Section: Discussionmentioning

confidence: 99%

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Analysis of microtubule sliding patterns inChlamydomonasflagellar axonemes reveals dynein activity on specific doublet microtubules

Wargo

McPeek

Smith

2004

Journal of Cell Science

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Generating the complex waveforms characteristic of beating eukaryotic cilia and flagella requires spatial regulation of dynein-driven microtubule sliding. To generate bending, one prediction is that dynein arms alternate between active and inactive forms on specific subsets of doublet microtubules. Using an in vitro microtubule sliding assay combined with a structural approach, we determined that ATP induces sliding between specific subsets of doublet microtubules, apparently capturing one phase of the beat cycle. These studies were also conducted using high Ca 2+ conditions. In Chlamydomonas, high Ca 2+ induces changes in waveform which are predicted to result from regulating dynein activity on specific microtubules. Our results demonstrate that microtubule sliding in high Ca 2+ buffer is also induced by dynein arms on specific doublets. However, the pattern of microtubule sliding in high Ca 2+ buffer significantly differs from that in low Ca 2+ . These results are consistent with a 'switching hypothesis' of axonemal bending and provide evidence to indicate that Ca 2+ control of waveform includes modulation of the pattern of microtubule sliding between specific doublets. In addition, analysis of microtubule sliding in mutant axonemes reveals that the control mechanism is disrupted in some mutants.

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Section: Resultsmentioning

confidence: 99%

Section: Sliding Pattern Correlates With Waveformmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

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Analysis of microtubule sliding patterns inChlamydomonasflagellar axonemes reveals dynein activity on specific doublet microtubules

Wargo

McPeek

Smith

2004

Journal of Cell Science

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“…It is possible that some second messengers affect motility by additional mechanisms that are independent of phosphorylation. For example, several subunits of dynein motors are EF-hand proteins that may bind calcium directly, altering dynein activity [Piperno et al, 1992;King and Patel-King, 1995;Yanagisawa and Kamiya, 2001;Casey et al, 2003;Guerra et al, 2003]. Chemical signaling also includes axonemal enzymes that are not directly sensitive to second messengers including casein kinase 1 (CK1), PP1, and PP2A, all of which appear to be involved in the control of dynein-driven motility [Walczak and Nelson, 1993; Central apparatus-associated polypeptides PF6 238-kDa alanine/proline rich protein; pf6 flagella lack the 1a projection on the C1 microtubule and display only twitching motion [Dutcher et al, 1984;Rupp et al, 2001] PF16 57-kDa armadillo repeat containing protein that localizes to the c1 microtubule; pf16 flagella lack the C1 microtubule and are paralyzed.…”

Section: Conserved Signaling Proteins Located In the Central Pair Andmentioning

confidence: 99%

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

Smith

Yang

2003

Cell Motil. Cytoskeleton

269

259

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“…DC1 and DC2 are coiled-coil proteins; they are essential for the OAD docking activity because mutants (oda1, oda3) lacking these proteins entirely lack OAD. In contrast, DC3 is a redox-sensitive Ca 2+ -binding protein and apparently is nonessential for OAD binding because a mutant (oda14) lacking it retains ∼40% of OADs (20,21). Presumably, DC3 has an as yet unidentified regulatory function.…”

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confidence: 99%

Cooperative binding of the outer arm-docking complex underlies the regular arrangement of outer arm dynein in the axoneme

Owa

Furuta

Usukura

et al. 2014

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

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Outer arm dynein (OAD) in cilia and flagella is bound to the outer doublet microtubules every 24 nm. Periodic binding of OADs at specific sites is important for efficient cilia/flagella beating; however, the molecular mechanism that specifies OAD arrangement remains elusive. Studies using the green alga Chlamydomonas reinhardtii have shown that the OAD-docking complex (ODA-DC), a heterotrimeric complex present at the OAD base, functions as the OAD docking site on the doublet. We find that the ODA-DC has an ellipsoidal shape ∼24 nm in length. In mutant axonemes that lack OAD but retain the ODA-DC, ODA-DC molecules are aligned in an end-to-end manner along the outer doublets. When flagella of a mutant lacking ODA-DCs are supplied with ODA-DCs upon gamete fusion, ODA-DC molecules first bind to the mutant axonemes in the proximal region, and the occupied region gradually extends toward the tip, followed by binding of OADs. This and other results indicate that a cooperative association of the ODA-DC underlies its function as the OAD-docking site and is the determinant of the 24-nm periodicity.C ilia and flagella of eukaryotic cells are organelles that generate fluid flow on the cell surface and/or sense chemical or mechanical stimuli from the external environment (1). Cilia/flagella beating is driven by outer arm dynein (OAD) and inner arm dyneins. The arrangement of dyneins on the axoneme has an overall periodicity of 96 nm, within which OAD binds every 24 nm; this 24-nm periodicity is completely conserved in essentially all eukaryotic organisms with "9 + 2" axonemes (2, 3) and even occurs in insect sperm flagella containing multiple rows of doublet microtubules arranged in a spiral configuration (4, 5). OAD is best characterized in Chlamydomonas. It is a very large protein complex of ∼2 MDa, comprising 3 heavy chains, 2 intermediate chains, and 11 distinct light chains. Most of the subunits are conserved from protists to mammals (6). OAD is the most abundant and most powerful axonemal dynein, generating about twothirds of the total propulsive force of ciliary beating (7,8). Human diseases due to ciliary motility defects [termed primary ciliary dyskinesia (PCD)] are caused most commonly by defects in OAD assembly (9-11). The assembly process and the in situ structure of the OAD complex in the axoneme have been well studied (3, 12, 13). However, the mechanism underlying the periodic binding of OAD to the doublet is poorly understood.The outer dynein arm-docking complex (ODA-DC) has been identified as a complex that mediates OAD binding to the doublet (14, 15). In the flagella of Chlamydomonas mutants (e.g., outerdynein-arm deficient oda6) retaining the ODA-DC but not OAD, the ODA-DC is observed by electron microscopy as a small projection linearly arrayed every 24 nm along the outer doublet (3,(14)(15)(16)(17). It is composed of three subunits: DC1, ∼83 kDa, encoded by ODA3; DC2, ∼62 kDa, encoded by ODA1; and DC3, ∼21 kDa, encoded by ODA14 (18-20), which assemble in the cell cytoplasm and are transported into the fla...

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DC3, the Smallest Subunit of the Chlamydomonas Flagellar Outer Dynein Arm-docking Complex, Is a Redox-sensitive Calcium-binding Protein

Cited by 44 publications

References 47 publications

Analysis of microtubule sliding patterns inChlamydomonasflagellar axonemes reveals dynein activity on specific doublet microtubules

Analysis of microtubule sliding patterns inChlamydomonasflagellar axonemes reveals dynein activity on specific doublet microtubules

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

Cooperative binding of the outer arm-docking complex underlies the regular arrangement of outer arm dynein in the axoneme

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