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Structure of a microtubule-bound axonemal dynein.

<div class='caption-title'>Structure of the ODA axonemal dynein bound to a doublet microtubule.</div>
<div class='caption-title'>The ODA complexes are in an apo state.</div>
<div class='caption-title'>Arrangement of the HC tails and IC–LC block and comparison with cytoplasmic dyneins.</div>
Walton T, Wu H, Brown A
OpenAccess logo Nat Commun 12 477 (2021)
Related entries: 7kzn, 7kzo

Cited: 28 times
EuropePMC logo PMID: 33473120

Abstract

Axonemal dyneins are tethered to doublet microtubules inside cilia to drive ciliary beating, a process critical for cellular motility and extracellular fluid flow. Axonemal dyneins are evolutionarily and biochemically distinct from cytoplasmic dyneins that transport cargo, and the mechanisms regulating their localization and function are poorly understood. Here, we report a single-particle cryo-EM reconstruction of a three-headed axonemal dynein natively bound to doublet microtubules isolated from cilia. The slanted conformation of the axonemal dynein causes interaction of its motor domains with the neighboring dynein complex. Our structure shows how a heterotrimeric docking complex specifically localizes the linear array of axonemal dyneins to the doublet microtubule by directly interacting with the heavy chains. Our structural analysis establishes the arrangement of conserved heavy, intermediate and light chain subunits, and provides a framework to understand the roles of individual subunits and the interactions between dyneins during ciliary waveform generation.

Articles - 7kzm mentioned but not cited (5)

  1. De novo identification of mammalian ciliary motility proteins using cryo-EM. Gui M, Farley H, Anujan P, Anderson JR, Maxwell DW, Whitchurch JB, Botsch JJ, Qiu T, Meleppattu S, Singh SK, Zhang Q, Thompson J, Lucas JS, Bingle CD, Norris DP, Roy S, Brown A. Cell 184 5791-5806.e19 (2021)
  2. Remodeling and activation mechanisms of outer arm dyneins revealed by cryo-EM. Kubo S, Yang SK, Black CS, Dai D, Valente-Paterno M, Gaertig J, Ichikawa M, Bui KH. EMBO Rep 22 e52911 (2021)
  3. ATP-induced conformational change of axonemal outer dynein arms revealed by cryo-electron tomography. Zimmermann N, Noga A, Obbineni JM, Ishikawa T. EMBO J 42 e112466 (2023)
  4. Axonemal structures reveal mechanoregulatory and disease mechanisms. Walton T, Gui M, Velkova S, Fassad MR, Hirst RA, Haarman E, O'Callaghan C, Bottier M, Burgoyne T, Mitchison HM, Brown A. Nature 618 625-633 (2023)
  5. Calaxin stabilizes the docking of outer arm dyneins onto ciliary doublet microtubule in vertebrates. Yamaguchi H, Morikawa M, Kikkawa M. Elife 12 e84860 (2023)


Reviews citing this publication (4)

  1. Composition and function of ciliary inner-dynein-arm subunits studied in Chlamydomonas reinhardtii. Yamamoto R, Hwang J, Ishikawa T, Kon T, Sale WS. Cytoskeleton (Hoboken) 78 77-96 (2021)
  2. Novel DNAH1 Mutation Loci Lead to Multiple Morphological Abnormalities of the Sperm Flagella and Literature Review. Zhuang BJ, Xu SY, Dong L, Zhang PH, Zhuang BL, Huang XP, Li GS, You YD, Chen D, Yu XJ, Chang DG. World J Mens Health 40 551-560 (2022)
  3. Structure Determination of Microtubules and Pili: Past, Present, and Future Directions. Garnett JA, Atherton J. Front Mol Biosci 8 830304 (2021)
  4. Formation and function of multiciliated cells. Lyu Q, Li Q, Zhou J, Zhao H. J Cell Biol 223 e202307150 (2024)

Articles citing this publication (19)

  1. Structure of dynein-dynactin on microtubules shows tandem adaptor binding. Chaaban S, Carter AP. Nature 610 212-216 (2022)
  2. Ciliary central apparatus structure reveals mechanisms of microtubule patterning. Gui M, Wang X, Dutcher SK, Brown A, Zhang R. Nat Struct Mol Biol 29 483-492 (2022)
  3. Cytoplasmic factories for axonemal dynein assembly. King SM. J Cell Sci 134 jcs258626 (2021)
  4. Electron microscopy for imaging organelles in plants and algae. Weiner E, Pinskey JM, Nicastro D, Otegui MS. Plant Physiol 188 713-725 (2022)
  5. Three-dimensional flagella structures from animals' closest unicellular relatives, the Choanoflagellates. Pinskey JM, Lagisetty A, Gui L, Phan N, Reetz E, Tavakoli A, Fu G, Nicastro D. Elife 11 e78133 (2022)
  6. Multi-curve fitting and tubulin-lattice signal removal for structure determination of large microtubule-based motors. Chai P, Rao Q, Zhang K. J Struct Biol 214 107897 (2022)
  7. Light chain 2 is a Tctex-type related axonemal dynein light chain that regulates directional ciliary motility in Trypanosoma brucei. Godar S, Oristian J, Hinsch V, Wentworth K, Lopez E, Amlashi P, Enverso G, Markley S, Alper JD. PLoS Pathog 18 e1009984 (2022)
  8. Outer-arm dynein light chain LC1 is required for normal motor assembly kinetics, ciliary stability, and motility. Sakato-Antoku M, King SM. Mol Biol Cell 34 ar75 (2023)
  9. Methylation of ciliary dynein motors involves the essential cytosolic assembly factor DNAAF3/PF22. Sakato-Antoku M, Patel-King RS, Balsbaugh JL, King SM. Proc Natl Acad Sci U S A 121 e2318522121 (2024)
  10. Microtubule-associated septin complexes modulate kinesin and dynein motility with differential specificities. Suber Y, Alam MNA, Nakos K, Bhakt P, Spiliotis ET. J Biol Chem 299 105084 (2023)
  11. Multi-omics approaches for comprehensive analysis and understanding of the immune response in the miniature pig breed. Arora D, Park JE, Lim D, Cho IC, Kang KS, Kim TH, Park W. PLoS One 17 e0263035 (2022)
  12. Novel compound heterozygous mutations in DNAH1 cause primary infertility in Han Chinese males with multiple morphological abnormalities of the sperm flagella. Wang M, Yang QY, Zhou JP, Tan HP, Hu J, Jin L, Zhu LX. Asian J Androl 25 512-519 (2023)
  13. Structural organization of the intermediate and light chain complex of Chlamydomonas ciliary I1 dynein. Fu G, Scarbrough C, Song K, Phan N, Wirschell M, Nicastro D. FASEB J 35 e21646 (2021)
  14. Structure of Motile Cilia. Ishikawa T. Subcell Biochem 99 471-494 (2022)
  15. News A structural model of the core of cilia. Nature (2023)
  16. N-Terminal Processing and Modification of Ciliary Dyneins. Sakato-Antoku M, Balsbaugh JL, King SM. Cells 12 2492 (2023)
  17. Regulation of motor activity of ciliary outer-arm dynein by the light chain 1; Implications from the structure of the light chain bound to the microtubule-binding domain of the heavy chain. Yagi T, Toda A, Ichikawa M, Kurisu G. Biophys Physicobiol 20 e200008 (2023)
  18. Splicing Mutation in DNALI1 Causes Male Infertility with Severe Oligoasthenoteratozoospermia in Humans. Zhang F, Li J, Liang Z, Chen X, Zheng H, Wu J, Chen W, Li L. Reprod Sci (2024)
  19. Torque generating properties of Tetrahymena ciliary three-headed outer-arm dynein. Yamaguchi S, Yamagishi M, Yajima J. Sci Rep 12 16722 (2022)


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