Regulatory mechanisms of sperm flagellar motility by metachronal and synchronous sliding of doublet microtubules

Abstract

STUDY QUESTION: What is the role of metachronal and synchronous sliding in sperm flagellar motility? SUMMARY ANSWER: Both metachronal and oscillatory synchronous sliding are essential for sperm flagellar motility, while the change in mode of synchronous sliding between the non-oscillatory synchronous sliding of a specific pair of the doublet microtubules and the oscillatory synchronous sliding between most pairs of doublet microtubules modulates the sperm flagellar motility. WHAT IS KNOWN ALREADY: Metachronal and synchronous sliding of doublet microtubules are involved in sperm flagellar motility and regulation of these sliding movements controls flagellar bend formation. STUDY DESIGN, SIZE, DURATION: To study the regulatory mechanisms of metachronal and synchronous sliding in flagellar movement of golden hamster spermatozoa, changes in these sliding movements during hyperactivation were examined by measuring the angle of the tangent to the flagellar shaft with reference to the central axis of the sperm head (the shear angle) along the flagellum. Golden hamster spermatozoa were obtained from the caudal epididymis of five sexually mature golden hamsters. Results from three experiments were averaged. The number of spermatozoa analyzed is 15 activated sperm, 22 hyperactivated sperm and 20 acrosome-reacted sperm. PARTICIPANTS/MATERIALS, SETTING, METHODS: For detailed field-by-field analysis, an individual flagellar image was tracked automatically using the Autotrace module of image analysis software. The coordinate values of the flagellar shaft were used to calculate the shear angle, which is proportional to the amount of microtubule sliding at any given position along the flagellum. The maximum shear angles of metachronal and synchronous sliding were obtained fromthe mean shear angles between the maximum shear angles of pro-hook bends and the absolute values of the minimum shear angles of anti-hook bends, which represent the amplitude of a set of successive shear angle curves, with 3-12 shear curves covering one beat cycle of sperm flagellar movement. Asymmetry of flagellar waves was expressed by the mean shear angle between the maximum shear angle of pro-hook bends and the minimum shear angle of anti-hook bends at 100 μm from the head-midpiece junction. MAIN RESULTS AND THE ROLE OF CHANCE: The asymmetrical flagellar movements observed in the activated (non-hyperactivated) and hyperactivated spermatozoa were characterized by the non-oscillatory synchronous sliding of a specific pair of the doublets; the large asymmetrical flagellar movement in the hyperactivated spermatozoa was generated by the large non-oscillatory synchronous sliding. Both the metachronal and synchronous sliding increased during the hyperactivation; however, the large symmetrical flagellar movement of the acrosome-reacted spermatozoa was characterized by the oscillatory synchronous sliding between most pairs of doublets. These results demonstrated that the metachronal and synchronous sliding are involved in generation and modulation of sperm flagellar motility; however, two types of synchronous sliding, non-oscillatory and oscillatory sliding, modulate the sperm flagellar motility by enhancing the sliding of a specific pair of the doublets or the sliding between most pairs of the doublets. LARGE SCALE DATA: None.LIMITATIONS, REASONS FOR CAUTION: This is an indirect study of the metachronal and synchronous sliding of doublet microtubules. Studies based on the direct observation of behavior of dynein are needed to clarify the sliding microtubule theory of flagellar movement of spermatozoa. WIDER IMPLICATIONS OF THE FINDINGS: Both the metachronal and oscillatory synchronous sliding of doublet microtubule generate and modulate sperm flagellar motility, while the change in mode of synchronous sliding between the non-oscillatory synchronous sliding and oscillatory synchronous sliding modulates the sperm flagellar motility. The coordination between these sliding leads to various types of flagellar and ciliary motility, including the asymmetrical beating in flagellar and ciliary movement and planar or helical beating in sea urchin spermatozoa. Moreover, the finding that the metachronal sliding and two types of synchronous sliding generate and modulate the flagellar motility will open a new avenue for quantitative analysis of flagellar and ciliary motility.STUDY FUNDING AND COMPETING INTEREST(S): The authors have no conflict of interest and no funding to declare.