The calcium‐induced curvature reversal of rat sperm is potentiated by cAMP and inhibited by anti‐calmodulin

Lindemann, Charles B.; Gardner, Tressa K.; Westbrook, Evonne; Kanous, Kathleen S.

doi:10.1002/cm.970200407

Cited by 42 publications

(28 citation statements)

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“…Further studies will determine which of the several NHE systems are functionally coupled to the Na,K-ATPase a4 isoform. Changes in pH have been shown to influence sperm motility, and in detergent-extracted preparations of rat sperm, variations in the proton concentration have been shown to modulate sperm flagellar bending pattern and its response to cAMP and Ca 2C (Lindemann et al 1991). Therefore, regulation of the proton concentration in the cells may represent one of the mechanism by which the Na,K-ATPase a4 isoform influences sperm motility.…”

Section: Discussionmentioning

confidence: 99%

Activity of the Na,K-ATPase α4 isoform is important for membrane potential, intracellular Ca2+, and pH to maintain motility in rat spermatozoa

Jiménez

Sánchez²,

Wertheimer³

et al. 2010

Reproduction

104

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While the function of the ubiquitous Na,K-ATPase a1 subunit has been well documented, the role of the sperm-specific a4 isoform of this ion transporter is less known. We have explored the importance of a4 in rat sperm physiology by taking advantage of the high sensitivity of this isoform for the inhibitor ouabain. Using concentrations that selectively block a4 activity, we found ouabain to reduce not only sperm total motility, but also multiple parameters of sperm movement, including progressive motility, straight line, curvilinear, and average path velocities, lateral head displacement, beat cross frequency, and linearity. According to a direct role of a4 in Na C transport, ouabain inhibition of a4 increased [Na C ] i in the male gametes. In addition, interference of a4 activity with ouabain produced cell membrane depolarization, diminished pH, and increased [Ca 2C ] i in spermatozoa. Inhibition of a4 was sufficient to cause all these effects and additional blockage of a1, the other Na,K-ATPase a isoform expressed in sperm, and higher doses of ouabain did not result in further changes in the cell parameters studied. These results show that a4 is the Na,K-ATPase isoform primarily involved in controlling the transmembrane Na C gradient in sperm, and that a4 activity is necessary for maintaining membrane potential, [Ca ] i , and acid-base balance suggests that their regulation is the mechanism by which a4 maintains motility of the male gametes.

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Section: Discussionmentioning

confidence: 99%

Activity of the Na,K-ATPase α4 isoform is important for membrane potential, intracellular Ca2+, and pH to maintain motility in rat spermatozoa

Jiménez

Sánchez²,

Wertheimer³

et al. 2010

Reproduction

104

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“…The hyperactivated motility pattern can be initiated in demembranated sperm by raising free Ca 21 levels from the range of pCa > 7 up to pCa 4 to 5 (Lindemann and Goltz, 1988;Lindemann and Kanous, 1989;Lindemann et al, 1991;Ishijima et al, 2006).…”

Section: Consequences Of Anatomy On Motilitymentioning

confidence: 99%

“…We now know that this conversion of the beating pattern requires the entry of Ca 21 for its initiation (Suarez and Osman, 1987) and maintenance (Carlson et al, 2009). The hyperactivated motility pattern can be initiated in demembranated sperm by raising free Ca 21 levels from the range of pCa > 7 up to pCa 4 to 5 (Lindemann and Goltz, 1988;Lindemann and Kanous, 1989;Lindemann et al, 1991;Ishijima et al, 2006).The greatly increased amplitude of the beat during hyperactivated motility necessitates that greater flagellar curvature is achieved, particularly in the midpiece. This is accompanied by greater sliding displacements of the doublets especially in the proximal part of the flagellum (Ishijima, 2007;Kaneko et al, 2007).…”

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confidence: 99%

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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“…In addition to the role of phosphorylation signalling in sperm motility, studies with a variety of species have shown that Ca 2+ ions play a key role in the development and maintenance of sperm progressive motion and hyperactivation (Lindemann et al, 1991;Serres et al, 1991;Marin-Briggiler et al, 1999;Marin-Briggiler et al, 2003;Marquez and Suarez, 2004). Using demembranated sperm models, some of these investigations have revealed that Ca 2+ levels modulate the waveform of the sperm tail (Ho et al, 2002;Lindemann and Goltz, 1988).…”

mentioning

confidence: 99%

Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation

Marı́n-Briggiler

Jha

Chertihin

et al. 2005

Journal of Cell Science

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The mechanisms involved in the regulation of mammalian sperm motility are not well understood. Calcium ions (Ca2+) have been suggested to play a key role in the maintenance of motility; nevertheless, how Ca2+ modulates this process has not yet been completely characterized. Ca2+ can bind to calmodulin and this complex regulates the activity of multiple enzymes, including Ca2+/calmodulin-dependent protein kinases (CaM kinases). Results from this study confirmed that the presence of Ca2+ in the incubation medium is essential for maintaining human sperm motility. The involvement of CaM kinases in Ca2+ regulation of human sperm motility was evaluated using specific inhibitors (KN62 and KN93) or their inactive analogues (KN04 and KN92 respectively). Sperm incubation in the presence of KN62 or KN93 led to a progressive decrease in the percentage of motile cells; in particular, incubation with KN62 also reduced sperm motility parameters. These inhibitors did not alter sperm viability, protein tyrosine phosphorylation or the follicular fluid-induced acrosome reaction; however, KN62 decreased the total amount of ATP in human sperm. Immunological studies showed that Ca2+/calmodulin-dependent protein kinase IV (CaMKIV) is present and localizes to the human sperm flagellum. Moreover, CaMKIV activity increases during capacitation and is inhibited in the presence of KN62. This report is the first to demonstrate the presence of CaMKIV in mammalian sperm and suggests the involvement of this kinase in the regulation of human sperm motility.

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The calcium‐induced curvature reversal of rat sperm is potentiated by cAMP and inhibited by anti‐calmodulin

Cited by 42 publications

References 42 publications

Activity of the Na,K-ATPase α4 isoform is important for membrane potential, intracellular Ca2+, and pH to maintain motility in rat spermatozoa

Activity of the Na,K-ATPase α4 isoform is important for membrane potential, intracellular Ca2+, and pH to maintain motility in rat spermatozoa

Functional anatomy of the mammalian sperm flagellum

Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation

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