Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants

Sun, Fei; Bahat, Anat; Gakamsky, Anna; Girsh, Eliezer; Katz, Nathan; Giojalas, Laura Cecilia; Tur-Kaspa, Ilan; Eisenbach, Michael

doi:10.1093/humrep/deh657

Cited by 130 publications

(105 citation statements)

References 28 publications

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“…It is widely acknowledged that spermatozoa in the human female reproductive tract have close and prolonged contact with a significant array of NO-producing cells (Rosselli et al 1998, Sun et al 2005, Machado-Oliveira et al 2008; the exact sites of NO production in the female genital tract remain to be investigated, but Machado-Oliveira et al (2008) showed that detectable amounts of NO are produced in human cumulus fragments and oviduct explants. This free radical is relatively unreactive, and is able to diffuse from the cell in which it is generated to the neighbor cells, covering long distances in a very short time (Krö ncke et al 1997).…”

Section: Discussionmentioning

confidence: 99%

Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway

Miraglia¹,

Angelis²,

Gazzano³

et al. 2011

Reproduction

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Nitric oxide (NO), a modulator of several physiological processes, is involved in different human sperm functions. We have investigated whether NO may stimulate the motility of human spermatozoa via activation of the soluble guanylate cyclase (sGC)/cGMP pathway. Sperm samples obtained by masturbation from 70 normozoospermic patients were processed by the swim-up technique. The kinetic parameters of the motile sperm-rich fractions were assessed by computer-assisted sperm analysis. After a 30-90 min incubation, the NO donor S-nitrosoglutathione (GSNO) exerted a significant enhancing effect on progressive motility (77, 78, and 78% vs 66, 65, and 62% of the control at the corresponding time), straight linear velocity (44, 49, and 48 mm/s vs 34, 35, and 35.5 mm/s), curvilinear velocity (81, 83, and 84 mm/s vs 68 mm/s), and average path velocity (52, 57, and 54 mm/s vs 40, 42, and 42 mm/s) at 5 mM but not at lower concentrations, and in parallel increased the synthesis of cGMP. A similar effect was obtained with the NO donor spermine NONOate after 30 and 60 min. The GSNO-induced effects on sperm motility were abolished by 1H-[1,2,4]oxadiazolo-[4,3-a]quinoxalin-1-one (a specific sGC inhibitor) and mimicked by 8-bromo-cGMP (8-Br-cGMP; a cell-permeating cGMP analog); the treatment with Rp-8-Br-cGMPS (an inhibitor of cGMP-dependent protein kinases) prevented both the GSNO-and the 8-Br-cGMP-induced responses. On the contrary, we did not observe any effect of the cGMP/PRKG1 (PKG) pathway modulators on the onset of hyperactivated sperm motility. Our results suggest that NO stimulates human sperm motility via the activation of sGC, the subsequent synthesis of cGMP, and the activation of cGMP-dependent protein kinases.

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Section: Discussionmentioning

confidence: 99%

Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway

Miraglia¹,

Angelis²,

Gazzano³

et al. 2011

Reproduction

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“…Sperm chemotaxis plays an essential role in species with external fertilization (Friedrich and Jülicher, 2007) and has been demonstrated to occur also in mammals (Sun et al, 2005). The process takes place in the proximity of the fertilization site and it is initiated by the release of factors from the oocyte and the surrounding cumulus cells.…”

Section: P-induced Sperm Chemotaxismentioning

confidence: 99%

Nongenomic activation of spermatozoa by steroid hormones: Facts and fictions

Baldi

Luconi

Muratori

et al. 2009

Molecular and Cellular Endocrinology

139

154

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a b s t r a c tThe rapid effects of steroids on spermatozoa have been demonstrated for the first time two decades ago. Progesterone (P), which is present throughout the female genital tract with peaks of levels in the cumulus matrix surrounding the oocyte, stimulates several sperm functions, including hyperactivation and acrosome reaction. These effects are mediated by an extranuclear pathway, as P stimulates an influx of calcium, the tyrosine phosphorylation of sperm proteins and other signalling cascades in a rapid manner. Whether these effects are receptor mediated and which receptors mediate these effects are still a matter of discussion despite all the efforts of the scientific community aimed at identifying them during the last 20 years. Although responsiveness to P is related to sperm fertilizing ability, the physiological role of P during the process of fertilization is discussed, and recent evidence points for a role of the steroid as a chemotactic agent for sperm. A similar situation applies for estrogens (E), which have been shown to induce direct effects on sperm by an extranuclear pathway. In particular, E appear to decrease acrosome reaction in response to P, exerting a role in ensuring an appropriate timing for sperm exocytosis during the process of fertilization.

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“…Although the attractants and the molecular mechanism of sperm chemotaxis in mammals are not yet known, sperm chemotaxis to follicular fluid, the mature oocyte and the surrounding cumulus oophorus have been reported by a number of studies (Jeon et al, 2001;Wang et al, 2001;Sun et al, 2005;Gil et al, 2008;Guidobaldi et al, 2008;Oren-Benaroya et al, 2008). It has been postulated that the chemoattractants, including heparin, progesterone, atrial natriuretic peptide (ANP), adrenaline, oxytocin, calcitonin and acetylcholine, might also be originated from the cumulus oophorus (Sliwa, 1993;Sliwa, 1994;Anderson et al, 1995;Sliwa, 1995;VillanuevaDíaz et al, 1995).…”

Section: Chemoattractants Released From Cumulus Cellsmentioning

confidence: 99%

Acrosome reaction in the cumulus oophorus revisited: involvement of a novel sperm-released factor NYD-SP8

2011

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Fertilization is a process involving multiple steps that lead to the final fusion of one sperm and the oocyte to form the zygote. One of the steps, acrosome reaction (AR), is an exocytosis process, during which the outer acrosome membrane fuses with the inner sperm membrane, leading to the release of acrosome enzymes that facilitate sperm penetration of the egg investments. Though AR has been investigated for decades, the initial steps of AR in vivo, however, remain largely unknown. A well elucidated model holds the view that AR occurs on the surface of the zona pellucida (ZP), which is triggered by binding of sperm with one of the ZP glycosylated protein, ZP3. However, this model fails to explain the large number of 'falsely' acrosome-reacted sperms found within the cumulus layer in many species examined. With the emerging evidence of cross-talk between sperm and cumulus cells, the potential significance of AR in the cumulus oophorus, the outer layer of the egg, has been gradually revealed. Here we review the acrosome status within the cumulus layer, the cross-talk between sperm and cumulus cells with the involvement of a novel spermreleased factor, NYD-SP8, and re-evaluate the importance and physiological significance of the AR in the cumulus in fertilization.

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Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants

Cited by 130 publications

References 28 publications

Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway

Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway

Nongenomic activation of spermatozoa by steroid hormones: Facts and fictions

Acrosome reaction in the cumulus oophorus revisited: involvement of a novel sperm-released factor NYD-SP8

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