Abstract
AXONEMAL dyneins have two or three globular heads joined by flexible tails to a common base, with each head/tail unit consisting of a single heavy-chain polypeptide of relative molecular mass >400,000. The sizes of the components have been deduced by electron microscopy1–3. The isolated β heavy chain of sea urchin sperm flagella, which is immunologically identical to that of the embryo cilia (data not shown; ref. 4), is of particular interest as it retains the capability for microtubule translocation in vitro5,6. Limited proteolysis of the β heavy chain divides it into two fragments, A and B, which sediment separately at 12S and 6S, and possibly correspond to the head and tail domains of the molecule7. Dynein ATPase is the energy-transducing enzyme that generates the sliding movement between tubules that underlies the beating of cilia and flagella of eukaryotes, and possibly also other large intracellular movements8,9. Here we report that the deduced amino-acid sequence of the β heavy chain of axonemal dynein from embryos of the sea urchin Tripneustes gratilla has 4,466 residues and contains the consensus motifs for five nucleotide-binding sites. The probable hydrolytic ATP-binding site can be identified by its location close to or at the VI site of vanadate-mediated photo-cleavage10. The general features of the map of photocleavage and proteolytic peptides reported earlier have been confirmed, except that the map's polarity is reversed. The predicted secondary structure of the β heavy chain consists of an α/β-type pattern along its whole length. The two longest regions of potential a. helix, with unbroken heptad hydrophobic repeats 120 and 50 amino acids long, may be of functional importance. But dynein does not seem to contain an extended coiled-coil tail domain.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Goodenough, U. W. & Heuser, J. J. molec. Biol. 180, 1083–1118 (1984).
Sale, W. S., Goodenough, U. W. & Heuser, J. E. J. Cell Biol. 101, 1400–1412 (1985).
Smith, E. F. & Sale, W. S. Cell Motil. Cytoskel. 18, 258–268 (1991).
Ogawa, K. et al. Cell Motil. Cytoskel. 16, 58–67 (1990).
Vale, R. D., Soll, D. R. & Gibbons, I. R. Cell 59, 915–925 (1989).
Sale, W. S., & Fox, L. A. J. Cell Biol. 107, 1793–1798 (1988).
Ow, R. A., Mocz, G., Tang, W.-J. Y. & Gibbons, I. R. J. biol. Chem. 262, 3409–3414 (1987).
Vale, R. D. A. Rev. Cell Biol. 3, 347–378 (1987).
Gibbons, I. R. J. biol. Chem. 263, 15837–15840 (1988).
Gibbons, I. R. et al. J. biol. Chem. 262, 2780–2786 (1987).
Mocz, G., Tang, W.-J. Y. & Gibbons, I. R. J. Cell Biol. 106, 1607–1614 (1988).
Ogawa, K. Proc. Japan Acad. 67B, 27–31 (1991).
Ogawa, K. Proc. Int. Echinoderm Cong. Tokyo (in the press).
Foltz, K. Asai, D. J., Cell Motil. Cytoskel. 16, 33–46 (1990).
Garber, A. T., Retief, J. D. & Dixon, G. H. EMBO J. 8, 1727–1734 (1989).
Walker, J. E., Saraste, M., Runswick, M. J. & Gay, N. J. EMBO J. 1, 945–951 (1982).
Cremo, C. R., Long, G. T. & Grammar, J. Biochemistry 29, 7982–7990 (1990).
Cremo, C. R. Biophys. J. 59, 513 (1991).
Gottesman, S., Clark, W. P. & Maurizi, M. R. J. biol. Chem. 265, 7886–7893 (1990).
Hayashi, M. & Higashi-Fujimi, S. Biochemistry 11, 2977–2982 (1972).
Mocz, G. & Gibbons, I. R. J. biol. Chem. 265, 2917–2922 (1990).
Tang, W.-J. Y. & Gibbons, I. R. J. biol. Chem. 262, 17728–17734 (1987).
King, S. M., Haley, B. E. & Witman, G. B. J. biol. Chem. 264, 10210–10218 (1989).
Gascuel, O. & Golmard, J. L. CABIOS 4, 357–365 (1988).
Mocz, G., Farias, J. & Gibbons, I. R. Biochemistry (in the press).
McLachlan, A. D. & Karn, J. J. molec. Biol. 164, 605–626 (1983).
Pearson, W. R. & Lipman, D. J. Proc. natn. Acad. Sci. U. S. A. 85, 2444–2448 (1988).
Obar, R. A., Collins, C. A., Hammarback, J. A., Shpetner, H. S. & Vallee, R. B. Nature 347, 256–261 (1990).
Warrick, H. M. & Spudich, J. A. A. Rev. Cell Biol. 3, 379–421 (1987).
Yang, J. T., Laymon, R. A. & Goldstein, L. S. B. Cell 56, 879–889 (1989).
Endow, S. A., Henikoff, S. & Soler-Niedziela, L. Nature 345, 81–83 (1990).
McDonald, H. B. & Goldstein, L. S. B. Cell 61, 991–1000 (1990).
Mocz, G. & Gibbons, I. R. Biochemistry 29, 4839–4843 (1990).
Gibbons, I. R. et al. Proc. natn. Acad. Sci. U.S.A. (in the press).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gibbons, I., Gibbons, B., Mocz, G. et al. Multiple nucleotide-binding sites in the sequence of dynein β heavy chain. Nature 352, 640–643 (1991). https://doi.org/10.1038/352640a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/352640a0
This article is cited by
-
CFAP45 deficiency causes situs abnormalities and asthenospermia by disrupting an axonemal adenine nucleotide homeostasis module
Nature Communications (2020)
-
A model for the chemomechanical coupling of the mammalian cytoplasmic dynein molecular motor
European Biophysics Journal (2019)
-
Sperm dysfunction and ciliopathy
Reproductive Medicine and Biology (2016)
-
Variation in DNAH1 may contribute to primary ciliary dyskinesia
BMC Medical Genetics (2015)
-
Structure of human cytoplasmic dynein-2 primed for its power stroke
Nature (2015)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.