Role of ions and ion channels in the regulation of Atlantic croaker sperm motility

Detweiler, Charles; Thomas, Peter

doi:10.1002/(sici)1097-010x(19980601)281:2<139::aid-jez8>3.0.co;2-p

Cited by 55 publications

(39 citation statements)

References 23 publications

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“…The increase in [Ca 2ϩ ] i under SMIF induction, which elicits circular motility, was 75% greater than that observed with 1͞2 NaF induction, which results in more linear motility. Differences in motility patterns are the result of [Ca 2ϩ ] i -associated flagellar bending, which becomes more asymmetric (circular motility) as [Ca 2ϩ ] i increases (7,36,39,40).…”

Section: Discussionmentioning

confidence: 99%

“…In salmonids, motility initiation occurs with dilution in freshwater, specifically from a reduction in extracellular potassium that drives a membrane hyperpolarization and an increase in intracellular calcium ([Ca 2ϩ ] i ) (2)(3)(4)(5)(6). Changes in the concentrations of specific ions (Ca 2ϩ , K ϩ , and possibly Na ϩ and Cl Ϫ ) also have been linked to motility initiation in Atlantic croaker sperm (7). A hyperpolarization of the sperm membrane also has been documented in carp sperm, reportedly linked to the opening of voltage-gated Ca 2ϩ channels and an increase in [Ca 2ϩ ] i (8).…”

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confidence: 99%

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Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Vines

Yoshida

Griffin

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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Sperm of the Pacific herring, Clupea pallasi, are unique in that they are immotile upon spawning in the environment. Herring sperm have evolved to remain motionless for up to several days after spawning, yet are still capable of fertilizing eggs. An egg chorion ligand termed ''sperm motility initiation factor'' (SMIF) induces motility in herring sperm and is required for fertilization. In this study, we show that SMIF induces calcium influx, sodium efflux, and a membrane depolarization in herring sperm. Sperm motility initiation by SMIF depended on decreased extracellular sodium (<350 mM) and could be induced in the absence of SMIF in very low sodium seawater. Motility initiation depended on > 1 mM extracellular calcium. Calcium influx caused by SMIF involved both the opening of voltage-gated calcium channels and reverse sodiumcalcium (Na ؉ ͞Ca 2؉ ) exchange. Membrane depolarization was slightly inhibited by a calcium channel blocker and markedly inhibited by a Na ؉ ͞Ca 2؉ exchange inhibitor. Sodium efflux caused by SMIF-initiated motility was observed when using both extracellular and intracellular sodium probes. A Na ؉ ͞Ca 2؉ exchange antigen was shown to be present on the surface of the sperm, primarily over the midpiece, by using an antibody to the canine Na ؉ ͞Ca 2؉ exchanger. This antibody recognized a 120-kDa protein that comigrated with the canine myocyte Na ؉ ͞Ca 2؉ exchanger. Sperm of Pacific herring are now shown to use reverse Na ؉ ͞Ca 2؉ exchange in motility initiation. This mechanism of regulation of motility initiation may have evolved for both maintenance of immotility after spawning as well as ligand-induced motility initiation.T eleost fish sperm are quiescent within the testes and seminal plasma before spawning, but most initiate motility after dilution into the external medium (freshwater or seawater for most species) in which spawning occurs (1). In salmonids, motility initiation occurs with dilution in freshwater, specifically from a reduction in extracellular potassium that drives a membrane hyperpolarization and an increase in intracellular calcium ([Ca 2ϩ ] i ) (2-6). Changes in the concentrations of specific ions (Ca 2ϩ , K ϩ , and possibly Na ϩ and Cl Ϫ ) also have been linked to motility initiation in Atlantic croaker sperm (7). A hyperpolarization of the sperm membrane also has been documented in carp sperm, reportedly linked to the opening of voltage-gated Ca 2ϩ channels and an increase in [Ca 2ϩ ] i (8). In other freshwater teleost sperm (goldfish, zebra fish), as well as in marine teleost sperm (puffer, flounder), motility is believed to occur as a result of nonspecific hypo-or hyperosmotic changes that drive changes in intracellular ion concentrations (5, 9, 10). Thus, in all systems studied to date, a membrane hyperpolarization leads to an increase in [Ca 2ϩ ] i and the initiation of motility.Although the stimulation of sperm motility in the vicinity of eggs has been reported in some teleost fish, only herring sperm have been shown to require an egg chorion-derived ligand for ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Vines

Yoshida

Griffin

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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“…In Atlantic croaker (Micropogonias undulatus), K + channel blockers reduced the percentage of motile cells (Detweiler and Thomas, 1998). In puffer fish it has been recently demonstrated that [K + ] i increased after sperm activation even after activation in potassium-free activation media (Gallego et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, Detweiler and Thomas (1998) have shown that although the sperm of Atlantic croaker was able to move in a medium without Ca 2+ , spermatozoa kinetic parameters were negatively affected by the depletion of this ion. Thus, it seems clear that there is a wide interspecific variability in relation to the presence/absence of extracellular ions and the effect thereof on the sperm motion parameters, so more studies focusing on this topic are necessary in order to design optimum species-specific activation media.…”

Section: Role Of Ions During the Sperm Activationmentioning

confidence: 99%

“…For example, while in species such as pufferfish, halibut, European sea bass or cod, sperm activation can be induced by hyperosmotic non-electrolyte solutions (e.g. glucose); in other species such as tilapia or Pacific herring extracellular Ca 2+ seems to be essential for the initiation of sperm motility.In addition, Detweiler and Thomas (1998) have shown that although the sperm of Atlantic croaker was able to move in a medium without Ca 2+ , GENERAL INTRODUCTION 15 spermatozoa kinetic parameters were negatively affected by the depletion of this ion. Thus, it seems clear that there is a wide interspecific variability in relation to the presence/absence of extracellular ions and the effect thereof on the sperm motion parameters, so more studies focusing on this topic are necessary in order to design optimum species-specific activation media.…”

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Sperm physiology and quality in two marine teleosts: Anguilla anguilla & Takifugu niphobles

Albiach¹

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ACKNOWLEDGEMENTSMuchos años han pasado desde que en aquel verano de 2007, cuando aún era un biólogo casi recién salido del horno, empecé mi carrera investigadora gracias a una beca en el grupo de investigación en el que hoy, unos años más viejuno, presento mi pequeña aportación a la ciencia. Durante todo este periodo he pasado buenos y malos momentos, mejores y peores rachas, pero sobretodo, he vivido una experiencia difícil de olvidar, o más bien inolvidable, en la que he podido madurar como persona y como investigador gracias a todas las personas que me han acompañado durante estos maravillosos años. Son muchos los agradecimientos que tengo que dar y poca la memoria, así que pido perdón por si alguien cae en el olvido, aunque no hay nada que no se pueda solucionar con una cerveza fresquita! En primer lugar, quería dar gracias a mi familia, que aunque nunca se lo diga y muchísimas veces parezca un "desapegao"… les quiero un montón. Ya hacen 33 primaveras que "el pare" y "la máaaama" (si, con acento) me trajeron al mundo, porque ya sabemos que lo que va primero es el oocito y el espermatozoide (Chapter 5… jjjjj), así que mil gracias por el cariño y el apoyo incondicional que me habéis dado durante todos estos años. En el mismo pack entra mi querida hermana "mongola" (uooooooooo… esto queda publicado en libro teta!!!), que también ha estado ahí y siempre me ha echado un cable cuando ha podido, aunque sea para decir… "tete no llegues tarde que mañana tienes laboratorio!!!" (si el microscopio o el citómetro hablaran...).A Paty (mi monito), por tu amor, comprensión y apoyo infinito durante todos estos años. Aún recuerdo el primer día que te conocí andando por el departamento y tu sonrisa se quedó grabada en mi memoria (que por cierto te invité a comer y me dijiste que… noooooooo!! toma xafun!!). Supongo que nos empezamos a querer en Monfragüe viendo y descubriendo pajarines mientras oíamos como cantaba el búhito, así que mil gracias por estar conmigo en los buenos y malos momentos, por ser un apoyo incondicional para mí, por quererme, y por todos estos años de sonrisas que hemos pasado juntos… que han sido muchos y muy bonitos.A mis amigos de toda la vida!!! Of course!!! que han estado ahí y estarán durante muchos años. Realmente es un grupo heterogéneo, que va desde los gorilillas de mi equipo de balonmano hasta algunos con los que empecé a gatear en preescolar. Que bien me lo he pasado en los torneos balonmaneros de San Esteve, donde dimos nuestros primeros pasos internacionales en materia de balonmano y en materia de bebercios!!! Mención especial merece mi amigo Caniggi, que a pesar de su estresante vida (tiene una pizzería, un huerto, un trabajo, un perro… y encima novia!!!) aun saca ratillos para jugar a pádel (hombre él jugar jugar… no juega… jjjjj) y recordad viejos tiempos de la infancia cuando aún éramos unos críos.Mucha gente es con la que he compartido laboratorio y a la que quería dar las gracias de manera especial. Realmente no estaría bien hablar de compañeros de laboratorio, porque ahora muchos de ell...

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Calcium‐induced quiescence of sperm motility in the bluegill (Lepomis macrochirus)

Zuccarelli¹,

Ingermann²

2007

J. Exp. Zool.

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Before dilution in hypoosmotic media sperm of freshwater fish are maintained quiescent by a range of factors including osmolality, K+ and pH, and the onset of motility is generally associated with an increase in cytoplasmic Ca2+. In contrast, Ca2+ in conjunction with osmolality was found to inhibit motility of intact bluegill sperm. Consistent with seminal plasma composition, 0.16 mmol/L Ca2+ and greater, in conjunction with an osmotic concentration of 290 mOsm/kg, inhibited the onset of bluegill sperm motility; sperm diluted in saline at 290 mOsm/kg without Ca2+ became motile. Cations Mn2+ and Sr2+, in conjunction with osmolality, had an inhibitory effect on initiation of sperm motility similar to that of Ca2+. Sperm motility was inhibited by Ca2+ channel blockers nimodipine and nifedipine, the mitochondrial Ca2+ uniporter inhibitor ruthenium red and the calmodulin inhibitors W-7 and trifluoperazine dihydrochloride. These results provide evidence that elevated cytoplasmic Ca2+ inhibits sperm motility and yet low levels permit or promote motility. This study demonstrates a unique inhibitory action of Ca2+ on the motility of intact fish sperm at physiologically relevant levels.

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Role of ions and ion channels in the regulation of Atlantic croaker sperm motility

Cited by 55 publications

References 23 publications

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Sperm physiology and quality in two marine teleosts: Anguilla anguilla & Takifugu niphobles

Calcium‐induced quiescence of sperm motility in the bluegill (Lepomis macrochirus)

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