The velocity of microtubule sliding: Its stability and load dependency

Abstract

It is now well understood that ATP-driven active sliding between the doublet microtubules in the sperm axoneme generates flagellar movement. However, much remains to be learned about how this movement is controlled. Detailed analyses of the flagellar beating of the mammalian spermatozoa revealed that there were two beating modes at a constant rate of microtubule sliding: that is, a nearly constant-curvature beating in nonhyperactivated spermatozoa and a nearly constant-frequency beating in hyperactivated spermatozoa. The constant rate of microtubule sliding suggests that the beat frequency and waveform of the flagellar beating are dependently regulated. Comparison of the sliding velocity of several mammalian and sea urchin sperm flagella with their mechanical property clarified that the sliding velocity of the microtubule was determined by the stiffness of the flagellum at its base, and that its relationship was expressed by a logarithmic equation that is similar to the classical force-velocity equation of the muscle contraction. Data from sea urchin spermatozoa also satisfied the equation, suggesting that the same microtubule sliding system functions in both the mammalian and echinoderm spermatozoa. Cell Motil. Cytoskeleton 64: 809-813, 2007

Emergence of flagellar beating from the collective behavior of individual ATP-powered dyneins

“…9b, where the curvature remains nearly constant as it propagates along the length of the axoneme, which is consistent with earlier findings [38,39]. Also, it is known that a nearly constant-curvature beating is characteristic for nonhyperactivated spermatozoa [59]. In Fig.…”

Dynamics of flagellar force generated by a hyperactivated spermatozoon

“…Furthermore, recent detailed analyses of flagellar movements of a spermatozoon using digital image processing revealed that the rate of microtubule sliding between doublet microtubules in the sperm flagella remained constant during the hyperactivation (Ishijima 2007), suggesting that the ATP concentration in the spermatozoon remains constant because the sliding velocity of the doublet microtubules is closely related to the ATP concentration (Gibbons & Gibbons 1972). These results also suggest that the propulsive thrust generated by a spermatozoon does not increase during the hyperactivation.…”

“…The low beat frequency in the hyperactivated spermatozoon resulted from its sharp bends of the sperm flagellum because the spermatozoon did not change the energy consumption during the hyperactivation (Ohmuro & Ishijima 2006, Ishijima 2007, Kaneko et al 2007). As seen in Table 1, the flagellar forces of the activated spermatozoon are not as low as those of the hyperactivated spermatozoon, suggesting that not the large flagellar waves but the low beat frequency is the most important feature of the hyperactivation.…”

Mechanical Constraint Converts Planar Waves into Helices on Tunicate and Sea Urchin Sperm Flagella

“…1) between the sea urchin and tunicate spermatozoa. In our earlier papers (Ishijima andHamaguchi, 1992, 1993;, we revealed that the proportion of spermatozoa yawing (or rolling) clockwise to those yawing (or rolling) counterclockwise was related to the Ca 2+ concentrations in the cell. Furthermore, the curvature of the circular swimming path or the asymmetrical flagellar waves was shown to correlate with the Ca 2+ concentration in the Ciona (Brokaw, 1997) and the sea urchin (Brokaw and Gibbons, 1975;Gibbons, 1982;Ishijima and Hamaguchi, 1993) spermatozoa in the same manner.…”

“…As a first step towards understanding the regulation of the localized active sliding between the doublet microtubules, the change in flagellar movement of mammalian spermatozoa has been analyzed in detail (Ishijima and Mohri, 1985;Ishijima et al, 2002;Ohmuro and Ishijima, 2006;Ishijima et al, 2006;Kaneko et al, 2007;Ishijima, 2007), because the mammalian spermatozoa remarkably change their flagellar movements in the female reproductive tract and its change in beating pattern is necessary for successful fertilization (Ishijima, 2007). Detailed examinations of the flagellar movements of mammalian spermatozoa revealed that there were two beating modes in flagellar movements under the constant rate of microtubule sliding; i.e., a constant sliding displacement mode generally observed in the normal spermatozoa and a constant frequency mode in the hyperactivated spermatozoa (Ohmuro and Ishijima, 2006;Ishijima, 2007). This change in flagellar movement of the hyperactivated spermatozoa resulted from a substantial increase in sliding displacement at the midpiece of the spermatozoa (Ohmuro and Ishijima, 2006).…”