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

Abstract

ABSTRACT. The change in the flagellar waves of spermatozoa from a tunicate and sea urchins was examined using high-speed video microscopy to clarify the regulation of localized sliding between doublet microtubules in the axoneme. When the tunicate Ciona spermatozoa attached to a coverslip surface by their heads in seawater or they moved in seawater with increased viscosity, the planar waves of the sperm flagella were converted into left-handed helical waves. On the other hand, conversion of the planar waves into helical waves in the sea urchin Hemicentrotus spermatozoa was not seen in seawater with an increased viscosity as well as in ordinary seawater. However, the sea urchin Clypeaster spermatozoa showed the conversion, albeit infrequently, when they thrust their heads into seawater with an increased viscosity. The chirality of the helical waves of the Clypeaster spermatozoa was right-handed. When Ciona spermatozoa swam freely near a glass surface, they moved in relatively large circular paths (yawing motion). There was no difference in the proportion of spermatozoa yawing in either a clockwise or counterclockwise direction when viewed from above, which was also different from that of the sea urchin spermatozoa. These observations suggest that the planar waves generally observed on the sperm flagella are mechanically regulated, although their stability must depend on the Ca 2+ concentration in the cell. Furthermore, the chirality of the helical waves may be determined by the intracellular Ca 2+ concentration and changed by transmitting the localized active sliding between the doublet microtubules around the axoneme in an alternative direction.

Regulations of Microtubule Sliding by Ca²⁺ and cAMP and Their Roles in Forming Flagellar Waveforms

“…helical waves (Ishijima, 2012). All spermatozoa (85 examples observed) demembranated under the potentially asymmetric condition also beat with planar waves when they were reactivated with MgATP 2-regardless of the Ca 2+ , cAMP, and MgATP 2-concentrations (Fig.…”

“…Furthermore, the planar waves of the tunicate and sea urchin sperm flagella convert to the helical waves at a slow beating in high viscosity media (Woolley and Vernon, 2001;Ishijima, 2012). These facts suggest that even if the all doublet microtubules are capable of sliding each other, the microtubule sliding that is ineffective for rapid beating is skipped, so that the localized active sliding discontinuously switches from one group of doublet microtubules to another and thus forms the planar waves.…”

“…In contrast, nodal cilia have a counterclockwise rotation when viewed from the base (Hirokawa et al, 2006) and this rotational movement produces a unidirectional nodal flow that triggers the L-R axis determination in the mammalian development. Careful observations of the effect of increased viscosity on the flagellar waves of tunicate and sea urchin spermatozoa revealed that the planar waves on the sperm flagella convert into the helical waves in seawater with an increased viscosity (Woolley and Vernon, 2001;Ishijima, 2012). This conversion seems to be related to the Ca 2+ and cAMP in the cell (Ishijima, 2012).…”

“…Careful observations of the effect of increased viscosity on the flagellar waves of tunicate and sea urchin spermatozoa revealed that the planar waves on the sperm flagella convert into the helical waves in seawater with an increased viscosity (Woolley and Vernon, 2001;Ishijima, 2012). This conversion seems to be related to the Ca 2+ and cAMP in the cell (Ishijima, 2012).…”

Sperm dysfunction and ciliopathy

“…The green alga Chlamydomonas has been used to generate many useful mutants for studying cilia and flagella, including mutants for the outer and inner dynein arms (oda and ida) [13,16] and other substructures (pf, paralyzed flagella) [17]. In animals, sperm from marine invertebrates have contributed to our understanding of the molecular architecture of flagella and the mechanism of their motility [18][19][20][21][22][23][24]. The molecular composition of axonemal dyneins has been widely examined in the green alga Chlamydomonas [25].…”