Volume regulation of mature and immature spermatozoa in a primate model, and possible ion channels involved

Yeung, Ching‐Hei; Barfield, Jennifer P.; Anapolski, Michael; Cooper, Trevor G.

doi:10.1093/humrep/deh466

Cited by 18 publications

(23 citation statements)

References 52 publications

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“…It has been reported for a variety of somatic cell types that the activation of the K C and Cl K channels is swelling sensitive, as is that of organic osmolyte channels (Lang et al 1998). Similar swelling-dependent activation of these channels has been demonstrated for spermatozoa of a variety of species such as cattle, swine, dog, and human (Kulkarni et al 1997, Petrunkina et al 2001a, 2004b, Barfield et al 2005, Yeung et al 2005a. The major candidates for these channels have been identified in boar and human sperm, in which the chloride channel (CLC)-3 of the CLC-family, the voltagegated K C channel Kv1.5, and the b-subunit minK protein appear to be the most likely to be involved (Petrunkina et al 2004a, Barfield et al 2005, Yeung et al 2005a.…”

Section: Mechanisms Of Cell Volume Regulationsupporting

confidence: 56%

“…During epididymal transit, an uptake of osmolytes from epididymal secretions takes place, and spermatozoa acquire the ability to regulate cell volume (Yeung et al 2004a). At ejaculation, they transfer from the hypertonic epididymal environment to the isotonic conditions of seminal plasma and the female genital tract fluids, at which time the spermatozoa experience a considerable osmotic gradient (Yeung et al 2004a(Yeung et al , 2004b and references therein). Moreover, under the artificial conditions of semen cryopreservation, the cells are exposed to major osmotic challenges: during freezing, they become dehydrated and shrink due to local hypertonicity; during thawing, when rehydration takes place, they are submitted to hypotonic shock.…”

Section: Physiological Importance Of Cell Volume Regulationmentioning

confidence: 99%

“…taurine flux). There are distinct differences in ion transport mechanisms between sperm of mouse, human, and domesticated species (Petrunkina et al 2001a, 2004b, Yeung et al 2004a, 2004b, 2005a, Klein et al 2006.…”

Section: Mechanisms Of Cell Volume Regulationmentioning

confidence: 99%

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Determinants of sperm quality and fertility in domestic species

Waberski²,

et al. 2007

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Fertilization success cannot be attributed solely to the absolute number of vital, motile, morphologically normal spermatozoa inseminated into the female but more especially to their functional competence. A range of in vitro tests has therefore been developed to monitor crucial aspects of sperm function: their ability to adapt to changing osmotic conditions, to bind to the oviductal epithelium, and to undergo capacitation in an appropriate and timely manner. The tests employ flow cytometry in conjunction with fluorescent techniques, electronic cell counting, and computer-assisted image area analysis. The highly quantitative analysis provided by electronic sizing and flow cytometry enables assessment of representative cell numbers in a very short time with high reproducibility. More importantly, it allows the detection of physiological heterogeneity within an ejaculate in terms of the development of cell subpopulations and enables the kinetic analysis of changes in living cell suspensions. The tests offer a promising strategy for evaluating fertility in domestic animals. The capability for volume regulation ensures that sperm recover from the tonic shocks experienced at ejaculation and during cryopreservation. Assessment of capacitation in vitro provides valuable information on both the sperm's ability to respond to fertilizing conditions and the sequence and rates of ongoing capacitation/destabilization processes. The monitoring of response to capacitating conditions in kinetic terms allows the sensitive and adequate detection of sperm populations expressing fertilization attributes and their ability to respond to external stimuli in a timely manner. However, subfertility is likely to be associated with a suboptimal response (i.e. too high or too low) rather than a minimal response.

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Section: Mechanisms Of Cell Volume Regulationsupporting

confidence: 56%

Section: Physiological Importance Of Cell Volume Regulationmentioning

confidence: 99%

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Determinants of sperm quality and fertility in domestic species

Waberski²,

et al. 2007

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“…However, it is not clear whether activation of GABA A receptor/Clchannel (GBRC) on the rat sperm by GABA and subsequent capacitation and hyperactivated motility involve extracellular HCO 3 À . In addition, it is known that Cl À and its channels play important roles in the maintenance of sperm cellular volume [Yeung et al 2004], intracellular pH [Zeng et al 1996], resting membrane potential and excitability [Chan et al 1997;Zhang and Shi 1998]. For example, the sperm cystic fibrosis transmembrane conductance regulator (CFTR) is a cAMP-activated Cl À channel which is involved in the transport of HCO 3 À that is important for sperm capacitation and fertilization [Hernandez-Gonzalez et al 2007;Xu et al 2007].…”

Section: Introductionmentioning

confidence: 99%

Activation of GABA_AReceptor/Cl⁻Channel and Capacitation in Rat Spermatozoa: HCO₃⁻and Cl⁻are Essential

Jin

Chen

Zhou

et al. 2009

Systems Biology in Reproductive Medicine

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This study was designed to determine whether HCO 3 À and Cl À are required for the activation of the GABA A receptor/Cl À channel (GBRC) by GABA and the subsequent capacitation of rat sperm. Spermatozoa from adult Sprague Dawley rats were incubated in four different media: modified complete rat fertilization medium (mRFM), Cl À -deficient (Cl À -DF) mRFM, HCO 3 À -DF mRFM, andCl À -DF HCO 3 À -DF mRFM, with or without GBRC agonists (GABA and progesterone) or GBRC antagonists (bicuculline and picrotoxin) for 0-6 h under capacitating conditions. Sperm capacitation and hyperactivation were assessed by chlortetracycline staining and computer-assisted sperm analysis, respectively. The results showed that GABA added to the mRFM accelerated capacitation and hyperactivation, followed by increase in the acrosome reaction, reaching maximum value after 5 h. Progesterone also accelerated sperm capacitation and hyperactivation. Bicuculline and picrotoxin, antagonists of GABA, blocked the effects of both GABA and progesterone acceleration of sperm capacitation and hyperactivation. Sperm capacitation required both Cl À and HCO 3 À . These results indicate that activation of GBRC may contribute to sperm capacitation and hyperactivation, and that both HCO 3 À and Cl À are essential. This is the first report of a close relationship between HCO 3 À /Cl À transport and the activation of GBRC in rat sperm capacitation and hyperactivation.

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“…Osmolytes and sperm volume regulation Although osmolyte levels have not been measured in immature (caput epididymidal) spermatozoa from the monkey and mouse, which are unable to perform RVD, 43,44 there are lower amounts of intracellular myo-inositol and glutamate in mature (cauda epididymidal) spermatozoa from infertile c-ros knockout (KO) mice, which are unable to control their volume, than those in the fertile heterozygous males, which can. 45 These observations are consistent with a role for organic osmolytes in regulating volume in mature sperm cells.…”

Section: Sperm Volume Regulation: the Fluid Environmentmentioning

confidence: 99%

The epididymis, cytoplasmic droplets and male fertility

Cooper¹

2010

Asian J Androl

146

130

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The potential of spermatozoa to become motile during post-testicular maturation, and the relationship between the cytoplasmic droplet and fertilizing capacity are reviewed. Post-testicular maturation of spermatozoa involves the autonomous induction of motility, which can occur in vivo in testes with occluded excurrent ducts and in vitro in testicular explants, and artefactual changes in morphology that appear to occur in the testis in vitro. Both modifications may reflect time-dependent oxidation of disulphide bonds of head and tail proteins. Regulatory volume decrease (RVD), which counters sperm swelling at ejaculation, is discussed in relation to loss of cytoplasmic droplets and consequences for fertility. It is postulated that: (i) fertile males possess spermatozoa with sufficient osmolytes to drive RVD at ejaculation, permitting the droplet to round up and pinch off without membrane rupture; and (ii) infertile males possess spermatozoa with insufficient osmolytes so that RVD is inadequate, the droplet swells and the resulting flagellar angulation prevents droplet loss. Droplet retention at ejaculation is a harbinger of infertility caused by failure of the spermatozoon to negotiate the uterotubal junction or mucous and reach the egg. In this hypothesis, the epididymis regulates fertility indirectly by the extent of osmolyte provision to spermatozoa, which influences RVD and therefore droplet loss. Man is an exception, because ejaculated human spermatozoa retain their droplets. This may reflect their short midpiece, approximating head length, permitting a swollen droplet to extend along the entire midpiece; this not only obviates droplet migration and flagellar angulation but also hampers droplet loss. Keywords: epididymis; fertility; infertility; sperm maturation INTRODUCTION During passage of mammalian spermatozoa through the epididymal duct, the functionally incompetent germ cell produced by the testis is matured and stored. In this time (around 1-2 weeks in most species), the spermatozoon undergoes many changes that prepare it for achieving the diverse tasks required of it. At ejaculation, when it is rapidly expelled from the epididymis through the vas deferens to the world outside, the spermatozoon undergoes another phase in which it encounters fluids of the male accessory sex glands, escapes from them in the vagina, cervix or uterus, depending on species, and interacts with the oviductal lining before fertilizing the female gamete. Many mechanisms control the timing of these events, all of which require adequate responses by the fertilizing spermatozoon, and several of these have their origins in the epididymis. This paper addresses a few controversial, novel or still unanswered topics related to the maturation, volume regulation and morphology of spermatozoa.

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Volume regulation of mature and immature spermatozoa in a primate model, and possible ion channels involved

Abstract: Quinine- and 4-AP-sensitive (implying K+) and NPPB-sensitive (implying Cl-) channels are involved in RVD of primate sperm, which develop this volume regulatory ability in the epididymis.

Cited by 18 publications

References 52 publications

Determinants of sperm quality and fertility in domestic species

Determinants of sperm quality and fertility in domestic species

Activation of GABA_AReceptor/Cl⁻Channel and Capacitation in Rat Spermatozoa: HCO₃⁻and Cl⁻are Essential

The epididymis, cytoplasmic droplets and male fertility

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Volume regulation of mature and immature spermatozoa in a primate model, and possible ion channels involved

Abstract: Quinine- and 4-AP-sensitive (implying K+) and NPPB-sensitive (implying Cl-) channels are involved in RVD of primate sperm, which develop this volume regulatory ability in the epididymis.

Cited by 18 publications

References 52 publications

Determinants of sperm quality and fertility in domestic species

Determinants of sperm quality and fertility in domestic species

Activation of GABAAReceptor/Cl−Channel and Capacitation in Rat Spermatozoa: HCO3−and Cl−are Essential

The epididymis, cytoplasmic droplets and male fertility

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Activation of GABA_AReceptor/Cl⁻Channel and Capacitation in Rat Spermatozoa: HCO₃⁻and Cl⁻are Essential