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Science 18 August 2006:
Vol. 313. no. 5789, pp. 944 - 948
DOI: 10.1126/science.1128618
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Research Articles

The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography

Daniela Nicastro,1*{dagger} Cindi Schwartz,1 Jason Pierson,1 Richard Gaudette,1 Mary E. Porter,2 J. Richard McIntosh1

Eukaryotic flagella and cilia are built on a 9 + 2 array of microtubules plus >250 accessory proteins, forming a biological machine called the axoneme. Here we describe the three-dimensional structure of rapidly frozen axonemes from Chlamydomonas and sea urchin sperm, using cryoelectron tomography and image processing to focus on the motor enzyme dynein. Our images suggest a model for the way dynein generates force to slide microtubules. They also reveal two dynein linkers that may provide "hard-wiring" to coordinate motor enzyme action, both circumferentially and along the axoneme. Periodic densities were also observed inside doublet microtubules; these may contribute to doublet stability.

1 Laboratory for 3D Electron Microscopy of Cells, Department of Molecular, Cellular, and Developmental Biology, CB 347, University of Colorado, Boulder, CO 80309–0347, USA.
2 Department of Genetics, Cell Biology, and Development, 6–160 Jackson Hall, 321 Church Street SE, University of Minnesota, Minneapolis, MN 55455, USA.

* Present address: Brandeis University, Rosenstiel, 415 South Street, Waltham, MA 02454, USA.

{dagger} To whom correspondence should be addressed. E-mail: nicastro{at}colorado.edu

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THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Partially Functional Outer-Arm Dynein in a Novel Chlamydomonas Mutant Expressing a Truncated {gamma} Heavy Chain.
Z. Liu, H. Takazaki, Y. Nakazawa, M. Sakato, T. Yagi, T. Yasunaga, S. M. King, and R. Kamiya (2008)
Eukaryot. Cell 7, 1136-1145
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High-Resolution Crystal Structure and In Vivo Function of a Kinesin-2 Homologue in Giardia intestinalis.
J. C. Hoeng, S. C. Dawson, S. A. House, M. S. Sagolla, J. K. Pham, J. J. Mancuso, J. Lowe, and W. Z. Cande (2008)
Mol. Biol. Cell 19, 3124-3137
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LRRC50, a Conserved Ciliary Protein Implicated in Polycystic Kidney Disease.
E. van Rooijen, R. H. Giles, E. E. Voest, C. van Rooijen, S. Schulte-Merker, and F. J. van Eeden (2008)
J. Am. Soc. Nephrol. 19, 1128-1138
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Dimeric heat shock protein 40 binds radial spokes for generating coupled power strokes and recovery strokes of 9 + 2 flagella.
C. Yang, H. A. Owen, and P. Yang (2008)
J. Cell Biol. 180, 403-415
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Three-dimensional structure of cytoplasmic dynein bound to microtubules.
N. Mizuno, A. Narita, T. Kon, K. Sutoh, and M. Kikkawa (2007)
PNAS 104, 20832-20837
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Kinesin-13 Regulates Flagellar, Interphase, and Mitotic Microtubule Dynamics in Giardia intestinalis.
S. C. Dawson, M. S. Sagolla, J. J. Mancuso, D. J. Woessner, S. A. House, L. Fritz-Laylin, and W. Z. Cande (2007)
Eukaryot. Cell 6, 2354-2364
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A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity.
E. E. Dymek and E. F. Smith (2007)
J. Cell Biol. 179, 515-526
   Abstract »    Full Text »    PDF »
Mechanical Properties of Inner-Arm Dynein-F (Dynein I1) Studied With In Vitro Motility Assays.
N. Kotani, H. Sakakibara, S. A. Burgess, H. Kojima, and K. Oiwa (2007)
Biophys. J. 93, 886-894
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Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites.
M. Cyrklaff, M. Kudryashev, A. Leis, K. Leonard, W. Baumeister, R. Menard, M. Meissner, and F. Frischknecht (2007)
J. Exp. Med. 204, 1281-1287
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Three-dimensional structures of the flagellar dynein-microtubule complex by cryoelectron microscopy.
T. Oda, N. Hirokawa, and M. Kikkawa (2007)
J. Cell Biol. 177, 243-252
   Abstract »    Full Text »    PDF »
Molecular Basis of Sperm Flagellar Axonemes: Structural and Evolutionary Aspects.
K. INABA (2007)
Ann. N.Y. Acad. Sci. 1101, 506-526
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Chlamydomonas Flagellar Outer Row Dynein Assembly Protein Oda7 Interacts with Both Outer Row and I1 Inner Row Dyneins.
J. Freshour, R. Yokoyama, and D. R. Mitchell (2007)
J. Biol. Chem. 282, 5404-5412
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Functional genomics in Trypanosoma brucei identifies evolutionarily conserved components of motile flagella.
D. M. Baron, K. S. Ralston, Z. P. Kabututu, and K. L. Hill (2007)
J. Cell Sci. 120, 478-491
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Dynein shifts into second gear.
M. P. Koonce (2006)
PNAS 103, 17587-17588
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Science. ISSN 0036-8075 (print), 1095-9203 (online)