Evidence for an increased sensitivity to Ca2+ in the flagella of sperm from tw32/+ mice

Lindemann, Charles B.; Goltz, Jason S.; Kanous, Kathleen S.; Gardner, Tressa K.; Olds‐Clarke, Patricia

doi:10.1002/mrd.1080260111

Cited by 26 publications

(12 citation statements)

References 34 publications

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“…By using the asymmetrical hook on the head of mouse sperm as a reference for the direction of the flagellar bend, we were able to identify two distinct kinds of asymmetrical beating. Procaine [24,[29][30][31][32], 4-AP [33,34], and thimerosal [21] are reported to trigger hyperactivation in the sperm of humans, guinea pigs, and cattle, but the response to thimerosal might actually be the reverse of the response to procaine and 4-AP.…”

Section: Discussionmentioning

confidence: 94%

Two Distinct Ca2+ Signaling Pathways Modulate Sperm Flagellar Beating Patterns in Mice1

Chang

Suárez

2011

Biology of Reproduction

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Hyperactivation, a swimming pattern of mammalian sperm in the oviduct, is essential for fertilization. It is characterized by asymmetrical flagellar beating and an increase of cytoplasmic Ca(2+). We observed that some mouse sperm swimming in the oviduct produce high-amplitude pro-hook bends (bends in the direction of the hook on the head), whereas other sperm produce high-amplitude anti-hook bends. Switching direction of the major bends could serve to redirect sperm toward oocytes. We hypothesized that different Ca(2+) signaling pathways produce high-amplitude pro-hook and anti-hook bends. In vitro, sperm that hyperactivated during capacitation (because of activation of CATSPER plasma membrane Ca(2+) channels) developed high-amplitude pro-hook bends. The CATSPER activators procaine and 4-aminopyridine (4-AP) also induced high-amplitude pro-hook bends. Thimerosal, which triggers a Ca(2+) release from internal stores, induced high-amplitude anti-hook bends. Activation of CATSPER channels is facilitated by a pH rise, so both Ca(2+) and pH responses to treatments with 4-AP and thimerosal were monitored. Thimerosal triggered a Ca(2+) increase that initiated at the base of the flagellum, whereas 4-AP initiated a rise in the proximal principal piece. Only 4-AP triggered a flagellar pH rise. Proteins were extracted from sperm for examination of phosphorylation patterns induced by Ca(2+) signaling. Procaine and 4-AP induced phosphorylation of proteins on threonine and serine, whereas thimerosal primarily induced dephosphorylation of proteins. Tyrosine phosphorylation was unaffected. We concluded that hyperactivation, which is associated with capacitation, can be modulated by release of Ca(2+) from intracellular stores to reverse the direction of the dominant flagellar bend and, thus, redirect sperm.

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Section: Discussionmentioning

confidence: 94%

Two Distinct Ca2+ Signaling Pathways Modulate Sperm Flagellar Beating Patterns in Mice1

Chang

Suárez

2011

Biology of Reproduction

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“…This is likely the explanation for the phenomenon of calcium arrest that has been observed in many types of cilia and flagella when subjected to high Ca 21 after demembranation and reactivation (Walter and Satir, 1978;Gibbons and Gibbons, 1980). Ca 21 arrest has been observed and studied with reactivated rat and mouse sperm (Lindemann and Goltz, 1988;Lindemann et al, 1990). The force exerted to maintain the arrest configuration has been shown to be generated by dynein (Lindemann et al, 1992;Moritz et al, 2001), but the absence of switching suggests that it is generated by a subset of dyneins that are constitutively activated in the presence of high Ca 21 .…”

Section: When Functional Anatomy Meets Physiologymentioning

confidence: 92%

Functional anatomy of the mammalian sperm flagellum

2016

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The eukaryotic flagellum is the organelle responsible for the propulsion of the male gamete in most animals. Without exception, sperm of all mammalian species use a flagellum for swimming. The mammalian sperm has a centrally located 9 1 2 arrangement of microtubule doublets and hundreds of accessory proteins that together constitute an axoneme. However, they also possess several characteristic peri-axonemal structures that make the mammalian sperm tail function differently. These modifications include nine outer dense fibers (ODFs) that are paired with the nine outer microtubule doublets of the axoneme, and are anchored in a structure called the connecting piece located at the base. The presence of the ODFs and connecting piece, and the absence of a basal body, dictate that physical forces generated by the dynein motors are transmitted to the base of the flagellum through the ODFs. Mammalian sperm flagella also possess a mitochondrial and a fibrous sheath that encircle most of the axoneme. These sheaths and the ODFs add mechanical rigidity to the flagellum creating the functional effect of increasing bend wavelength, which requires the entrainment of more dynein motors in the production of a single wave. The sheaths also act as a retinaculum and maintain the integrity of the central axoneme when large bending torques are generated by dynein. Large torque production is crucial to the process of hyperactivation and the unique motility transitions associated with effective fertilizing capacity. Consequently, these specialized anatomical features are essential for the effective interaction of sperm with the female reproductive tract and ovum. V C 2016 Wiley Periodicals, Inc.Key Words: axoneme; outer dense fibers; fibrous sheath; outer doublets; dynein; connecting piece; hyperactivation; sperm motility Introduction E ukaryotic cilia and flagella are highly conserved and ubiquitous organelles present in most animals, as well as many lower plants and eukaryotic protozoa. In the vertebrate lineage, the eukaryotic flagellum is universally employed to propel the male gamete. In the mammalian branch of the vertebrates, the sperm tail is always a modified flagellum with some characteristic accessory features that are added onto the basic 9 1 2 axoneme of microtubules found in most cilia and flagella. Figure 1 shows transmission electron micrographs (TEMs) of a mouse sperm flagellum in cross section at several positions along the length of the flagellum. The central axoneme is visible with its nine outer doublets surrounding a pair of single central microtubules (central pair or CP). Each of the outer microtubule doublets bears two rows of projections called the inner row and outer row of dynein arms. These arms are composed of the dynein motor proteins that power motility. The dynein arms are the source of the motive force that bends the flagellum. The dynein heavy chains (DHC) of the arms form bridges between the outer doublets and undergo a Mg-ATP driven power stroke that generates a sliding (or shearing) action between t...

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“…It was demonstrated that the response to Ca 2ϩ at high concentration leads to the arrest of flagellar beating at one extreme of the beat cycle. This produces candy-cane-shaped arrested flagella in sea urchin sperm [Gibbons, 1980;Gibbons and Gibbons, 1980] and fishhook-shaped arrested flagella in rat and mouse sperm [Lindemann and Goltz, 1988;Lindemann et al, 1990], as seen in Figure 1. Cilia also show arrest of the beat cycle in response to Ca 2ϩ [Satir, 1975;Satir et al, 1976], and the "hands up" arrest pattern is surprisingly similar to the fishhook of rat sperm [Satir et al, 1991].…”

Section: Introductionmentioning

confidence: 93%

Direct measurement of the passive stiffness of rat sperm and implications to the mechanism of the calcium response

Schmitz-Lesich

Lindemann

2004

Cell Motil. Cytoskeleton

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Glass microprobes were used to measure the stiffness of the flagella of Triton X-100-extracted rat sperm models. The sperm models were treated with 50 microM sodium vanadate and 0.1 mM Mg-ATP to evaluate the stiffness of the passive flagellar structure without the influence of the dynein motor proteins. The passive stiffness was determined to be 4.6 (+/- 1.1) x 10(-19) N x m(2). Rat sperm models exposed to greater than 10(-5) M calcium ions exhibit a strong bend in the basal 40 microm of the flagellum, resulting in a fishhook-like appearance. The torque required to bend a passive rat sperm flagellum into the fishhook-like configuration was determined. The result was compared to the previously published measurement of the torque required to straighten the flagella of rat sperm in the Ca(2+)-induced fishhook configuration [Moritz et al., 2001: Cell Motil. Cytoskeleton 49:33-40]. The torque required to induce a fishhook in a passive flagellum was 2.7 (+/- 0.7) x 10(-14) N x m and the torque to straighten an active Ca(2+)-induced fishhook was 2.6 (+/- 1.4) x 10(-14) N x m. These values are identical within the limit of error of the measurement technique. This finding suggests that the fishhook configuration observed in the Ca(2+) response of rat sperm is the result of a Newtonian equilibrium, where active torque produced by dynein is counterbalanced by an equal and opposite passive torque that results from bending the flagellum. Consistent with this mechanism, the Ca(2+)-induced fishhook configuration is progressively relaxed by incremental increases in sodium vanadate concentration. This supports an active role of the dynein motors in producing the torque for the response. When rat sperm respond to Ca(2+), the bend in the flagellum always forms in the direction opposite the curvature of the asymmetric sperm head. Based on this polarity, the bending torque for the Ca(2+) response must result from the action of the dyneins on outer doublets 1 through 4.

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Evidence for an increased sensitivity to Ca²⁺ in the flagella of sperm from t^w32/+ mice

Cited by 26 publications

References 34 publications

Two Distinct Ca2+ Signaling Pathways Modulate Sperm Flagellar Beating Patterns in Mice1

Two Distinct Ca2+ Signaling Pathways Modulate Sperm Flagellar Beating Patterns in Mice1

Functional anatomy of the mammalian sperm flagellum

Direct measurement of the passive stiffness of rat sperm and implications to the mechanism of the calcium response

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