Zn2+ induces hyperpolarization by activation of a K+ channel and increases intracellular Ca2+ and pH in sea urchin spermatozoa

Beltrán, Carmen; Rodríguez‐Miranda, Esmeralda; Granados-González, Gisela; Torre, Lucia García de De la; Nishigaki, Takuya; Darszon, Alberto

doi:10.1016/j.ydbio.2014.07.017

Cited by 20 publications

(15 citation statements)

References 60 publications

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“…Sea urchin spermatids are normally ejaculated into sea water, and diluting them into sea water triggers activation and sperm motility [ 34 ]. Further studies demonstrated that zinc is the active ingredient in sea water and that zinc causes an increase in intracellular pH and intracellular calcium levels, triggering the acrosome reaction, a membrane fusion event [ 34 , 35 ]. However, the mechanism by which zinc activates sea urchin sperm has not been defined, and no zinc transporters have thus far been implicated.…”

Section: Discussionmentioning

confidence: 99%

The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes

et al. 2018

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Sperm activation is a fascinating example of cell differentiation, in which immotile spermatids undergo a rapid and dramatic transition to become mature, motile sperm. Because the sperm nucleus is transcriptionally silent, this transition does not involve transcriptional changes. Although Caenorhabditis elegans is a leading model for studies of sperm activation, the mechanisms by which signaling pathways induce this transformation remain poorly characterized. Here we show that a conserved transmembrane zinc transporter, ZIPT-7.1, regulates the induction of sperm activation in Caenorhabditis nematodes. The zipt-7.1 mutant hermaphrodites cannot self-fertilize, and males reproduce poorly, because mutant spermatids are defective in responding to activating signals. The zipt-7.1 gene is expressed in the germ line and functions in germ cells to promote sperm activation. When expressed in mammalian cells, ZIPT-7.1 mediates zinc transport with high specificity and is predominantly located on internal membranes. Finally, genetic epistasis places zipt-7.1 at the end of the spe-8 sperm activation pathway, and ZIPT-7.1 binds SPE-4, a presenilin that regulates sperm activation. Based on these results, we propose a new model for sperm activation. In spermatids, inactive ZIPT-7.1 is localized to the membranous organelles, which contain higher levels of zinc than the cytoplasm. When sperm activation is triggered, ZIPT-7.1 activity increases, releasing zinc from internal stores. The resulting increase in cytoplasmic zinc promotes the phenotypic changes characteristic of activation. Thus, zinc signaling is a key step in the signal transduction process that mediates sperm activation, and we have identified a zinc transporter that is central to this activation process.

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Section: Discussionmentioning

confidence: 99%

The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes

et al. 2018

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“…Sperm fluorescence measurements were done as described 60 with a 5 μ l aliquot of Fluo-4 labelled sperm (diluted 1:5 in 1CaASW pH 7.0) added to a round cuvette containing 800 μ l ASW at 14 °C under constant stirring in a SLM 8000 Aminco spectrofluorometer. Fluo-4 has been used to detect speract induced [ Ca 2+ ] i oscillations in individual sea urchin sperm and in populations.…”

Section: Methodsmentioning

confidence: 99%

Network model predicts that CatSper is the main Ca2+ channel in the regulation of sea urchin sperm motility

Espinal-Enríquez

Priego-Espinosa

Darszon

et al. 2017

Sci Rep

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Spermatozoa sea urchin swimming behaviour is regulated by small peptides from the egg outer envelope. Speract, such a peptide, after binding to its receptor in Strongylocentrotus purpuratus sperm flagella, triggers a signaling pathway that culminates with a train of intracellular calcium oscillations, correlated with changes in sperm swimming pattern. This pathway has been widely studied but not fully characterized. Recent work on Arbacia punctulata sea urchin spermatozoa has documented the presence of the Ca2+ CatSper channel in their flagella and its involvement in chemotaxis. However, if other calcium channels participate in chemotaxis remains unclear. Here, based on an experimentally-backed logical network model, we conclude that CatSper is fundamental in the S. purpuratus speract-activated sea urchin sperm signaling cascade, although other Ca2+ channels could still be relevant. We also present for the first time experimental corroboration of its active presence in S. purpuratus sperm flagella. We argue, prompted by in silico knock-out calculations, that CatSper is the main generator of calcium oscillations in the signaling pathway and that other calcium channels, if present, have a complementary role. The approach adopted here allows us to unveil processes, which are hard to detect exclusively by experimental procedures.

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“…Sperm hyperactivation induced by Ca ion influx is promoted by membrane depolarization in media rich in extracellular K ions [ 21 ] (and other depolarizing agents), or by membrane hyperpolarization through the activation of Slo3 channels [ 3 , 23 ], possibly induced by Zn ions [ 18 ]. Both processes require alkaline media.…”

Section: Discussionmentioning

confidence: 99%

“…This mechanism enables a greater ROS activity necessary for motility induction, both progressive and hyperactivated. Considerably recent evidence suggest that submicromolar concentrations of free Zn 2+ hyperpolarizes sea urchin sperm membrane potential by activation of a K+ channel (Slo3) and increase the concentration of intracellular Ca 2+ [ 18 ]. It is possible that mammalian sperm also possess the similar mechanism of Ca 2+ entry.…”

Section: Introductionmentioning

confidence: 99%

Synergetic Effects of K, Ca, Cu and Zn in Human Semen in Relation to Parameters Indicative of Spontaneous Hyperactivation of Spermatozoa

et al. 2016

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We have observed that sperm quality parameters indicative of spermatozoa hyperactivation such are lower “linearity” and “straightness”, and as showed by this research “elongation”, were more pronounced in patients with normal spermiogram compared to the group of men with reduced sperm motility who were undergoing routine in vitro fertilisation. The research encompassed 97 men diagnosed with normozoospermia (n = 20), asthenozoospermia (n = 54) and oligoasthenozoospermia (n = 23). The findings indicate that sperm quality of patients with normal spermiogram diagnosed according to WHO criteria, may be compromised by showing premature spontaneous hyperactivation which can decrease the chances of natural conception. We assessed synergistic effects of multiple chemical elements in ejaculated semen to find if premature spontaneous hyperactivation of spermatozoa can be a sign of imbalanced semen composition especially of elements K, Ca, Cu and Zn. Human semen samples showing low or high baseline status of chemical elements concentrations were found in samples from all three diagnostic groups. However, correlation of K/Ca and Cu/Zn ratios, taking into account samples from all three groups of men, were negative at statistical significance level p = 0.01. We tested if the negative correlation between K/Ca and Cu/Zn ratio works for greater number of semen samples. We found the negative correlation to be valid for 175 semen samples at statistical significance of p = 0.00002. The ratio of K/Ca and Cu/Zn, i.e. increased concentrations of K and Zn in comparison to concentrations of Ca and Cu, were associated with a decrease of “straightness” in the group of men with normal spermiogram and pronounced spontaneous hyperactivation of spermatozoa, implying that these elements act in synergy and that the balance of elements and not their absolute concentrations plays the major role in premature spermatozoa hyperactivation in ejaculated semen.

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Zn2+ induces hyperpolarization by activation of a K+ channel and increases intracellular Ca2+ and pH in sea urchin spermatozoa

Cited by 20 publications

References 60 publications

The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes

The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes

Network model predicts that CatSper is the main Ca2+ channel in the regulation of sea urchin sperm motility

Synergetic Effects of K, Ca, Cu and Zn in Human Semen in Relation to Parameters Indicative of Spontaneous Hyperactivation of Spermatozoa

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