High-frequency nanometre-scale vibration in 'quiescent' flagellar axonemes

THE movement of cilia and flagella is based on the interaction between dynein arms and microtubules coupled with ATP hydroly-sis. Although it is established that dynein arms cause adjacent microtubules to slide, little is known about the elementary process underlying the force production. To look more closely at the mechano-chemical conversion mechanism, we recently developed an optical method for measuring a nanometre-scale displacement with a time-resolution better than 1 ms. We now report the detection of high frequency ( ∼ 300 Hz) vibration of sub-nanometre ampli-tude in non-beating flagellar axonemes. This vibration could reflect the movement of individual activated dynein arms.

[1]  W. Sale The axonemal axis and Ca2+-induced asymmetry of active microtubule sliding in sea urchin sperm tails , 1986, The Journal of cell biology.

[2]  W. Sale,et al.  Direction of active sliding of microtubules in Tetrahymena cilia. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[3]  K. Oiwa,et al.  The force-velocity relationship for microtubule sliding in demembranated sperm flagella of the sea urchin. , 1988, Cell structure and function.

[4]  I. Gibbons,et al.  Calcium-induced quiescence in reactivated sea urchin sperm , 1980, The Journal of cell biology.

[5]  C. Brokaw,et al.  Mechanochemical coupling in flagella. V. Effects of viscosity on movement and ATP-dephosphorylation of Triton-demembranated sea-urchin spermatozoa. , 1977, Journal of cell science.

[6]  M. Sheetz,et al.  Tracking kinesin-driven movements with nanometre-scale precision , 1988, Nature.

[7]  H. Shimizu,et al.  A model of flagellar movement based on cooperative dynamics of dynein-tubulin cross-bridges. , 1986, Journal of theoretical biology.

[8]  I. Gibbons,et al.  Acetate anions stabilize the latency of dynein 1 ATPase and increase the velocity of tubule sliding in reactivated sperm flagella. , 1982, Progress in clinical and biological research.

[9]  C. Brokaw Elastase digestion of demembranated sperm flagella , 1980, Science.

[10]  I. Gibbons,et al.  FLAGELLAR MOVEMENT AND ADENOSINE TRIPHOSPHATASE ACTIVITY IN SEA URCHIN SPERM EXTRACTED WITH TRITON X-100 , 1972, The Journal of cell biology.

[11]  S Kamimura,et al.  Direct measurement of nanometric displacement under an optical microscope. , 1987, Applied optics.

[12]  T. Miki-Noumura,et al.  Sliding velocity between outer doublet microtubules of sea-urchin sperm axonemes. , 1980, Journal of cell science.

[13]  K. Johnson Pathway of the microtubule-dynein ATPase and the structure of dynein: a comparison with actomyosin. , 1985, Annual Review of Biophysics and Biophysical Chemistry.

[14]  R. Fettiplace,et al.  The mechanical properties of ciliary bundles of turtle cochlear hair cells. , 1985, The Journal of physiology.

[15]  I. Mabuchi,et al.  Activation of sea urchin sperm flagellar dynein ATPase activity by salt-extracted axonemes. , 1987, Journal of biochemistry.

[16]  I. Gibbons,et al.  Organic anions stabilize the reactivated motility of sperm flagella and the latency of dynein 1 ATPase activity , 1985, The Journal of cell biology.

[17]  A J Hudspeth,et al.  Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[18]  I. Gibbons,et al.  A latent adenosine triphosphatase form of dynein 1 from sea urchin sperm flagella. , 1979, The Journal of biological chemistry.

[19]  D. Goldstein Calculation of the concentrations of free cations and cation-ligand complexes in solutions containing multiple divalent cations and ligands. , 1979, Biophysical journal.

[20]  C. Omoto,et al.  Activation of the dynein adenosinetriphosphatase by microtubules. , 1986, Biochemistry.

[21]  K. Johnson,et al.  Presteady state kinetic analysis of vanadate-induced inhibition of the dynein ATPase. , 1983, Journal of Biological Chemistry.

[22]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[23]  W. Sale,et al.  Potent inhibition of dynein adenosinetriphosphatase and of the motility of cilia and sperm flagella by vanadate. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. Brokaw,et al.  Mechanochemical coupling in flagella. I. Movement-dependent dephosphorylation of ATP by glycerinated spermatozoa. , 1968, Archives of biochemistry and biophysics.

[25]  B. Anner,et al.  Rapid determination of inorganic phosphate in biological systems by a highly sensitive photometric method. , 1975, Analytical biochemistry.