The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCζ

Swann, Karl; Larman, Mark G.; Saunders, Christopher P.; Lai, F. Anthony

doi:10.1530/rep.1.00169

Cited by 154 publications

(94 citation statements)

References 62 publications

(43 reference statements)

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“…Subsequent IP 3 binding to its own receptor on the endoplasmic reticulum (ER) [19] opens Ca 2+ channels, which release Ca 2+ from the ER into the cytoplasm of the oocyte [19]. The resulting Ca 2+ oscillations within the oocyte [18,19] disseminate from the cortical region throughout the ooplasm [20,21] at 10-to 20-min intervals [22], triggering oocyte activation [23] to initiate oocyte fertilization and preimplantation embryogenesis [8,14,17].…”

Section: Discussionmentioning

confidence: 99%

Phospholipase C-zeta deficiency as a cause for repetitive oocyte fertilization failure during ovarian stimulation for in vitro fertilization with ICSI: a case report

Chithiwala

Lee

Hill

et al. 2015

J Assist Reprod Genet

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Purpose The purpose of this study is to describe impaired oocyte fertilization from phospholipase C-zeta (PLC-ζ) deficiency in normal-appearing sperm that was successfully treated using calcium (Ca 2+ ) ionophore with intracytoplasmic sperm injection (ICSI) of oocytes matured in vitro. Methods An infertile couple undergoing in vitro fertilization (IVF) experienced failed oocyte fertilization following ICSI with normal-appearing sperm. A semen sample collected from the patient was used to assess the expression of sperm PLC-ζ protein by Western blot analysis and immunofluorescence and PLC-ζ bioactivity by an in vitro model of Ca 2+ release. A second IVF cycle was performed using Ca 2+ ionophore with ICSI to enhance Ca 2+ -induced oocyte activation of oocytes matured in vitro.Results Sperm PLC-ζ protein deficiency was demonstrated by Western blot analysis and immunofluorescence and confirmed by reduced PLC-ζ bioactivity using an in vitro model of Ca 2+ release. Nevertheless, with this sperm and supplementation of Ca 2+ ionophore following ICSI, fertilization of four of six oocytes matured in vitro was obtained. In addition, four embryos underwent cleavage and two of them reached the blastocyst stage. Transfer of these blastocysts into the uterus led to a single pregnancy and live birth. Conclusions Deficiency of PLC-ζ in normal-appearing human sperm is associated with impaired Ca 2+ -dependent oocyte activation during ICSI. Under this condition, use of Ca 2+ ionophore following ICSI of oocytes matured in vitro improves embryo developmental competence, possibly through the activation of Ca 2+ -dependent mechanisms governing fertilization and preimplantation embryogenesis.

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Section: Discussionmentioning

confidence: 99%

Phospholipase C-zeta deficiency as a cause for repetitive oocyte fertilization failure during ovarian stimulation for in vitro fertilization with ICSI: a case report

Chithiwala

Lee

Hill

et al. 2015

J Assist Reprod Genet

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“…Quick disintegration of the sperm plasma membrane within the oocyte is important because oocyte activation depends on sperm-borne oocyte-activating factor (SOAF). The strongest candidate for SOAF in mammals thus far is phospholipase C- (17)(18)(19)(20). At least part of SOAF is localized in the perinuclear theca in the postacrosomal region (21)(22)(23)(24) and under the plasma membrane over the equatorial segment of the acrosome (25).…”

Section: Discussionmentioning

confidence: 99%

Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development

Morozumi

Shikano

Miyazaki

et al. 2006

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

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Direct injection of a single spermatozoon into an oocyte (ICSI) can produce apparently normal offspring. Although the production of normal offspring by ICSI has been successful in mice and humans, it has been less successful in many other species. The reason for this is not clear, but could be, in part, due to inconsistent activation of oocytes because of delayed disintegration of sperm plasma membrane within oocytes and incorporation of the acrosome containing a spectrum of hydrolyzing enzymes. In the mouse, the removal of sperm plasma membrane and acrosome was not a prerequisite to produce offspring by ICSI, but it resulted in earlier onset of oocyte activation and better embryonic development. The best result was obtained when spermatozoa were demembranated individually immediately before ICSI by using lysolecithin, a hydrolysis product of membrane phospholipids.mouse ͉ human ͉ Ca 2ϩ oscillations ͉ fertilization ͉ lysolecithin D irect injection of a single spermatozoon into an oocyte, commonly called intracytoplasmic sperm injection (ICSI), can produce apparently normal offspring even though it bypasses a number of biological processes necessary for normal fertilization. As long as the sperm nucleus has intact genetic integrity, ICSI can produce healthy offspring regardless of concentrations, morphology, and motility of spermatozoa (1, 2). Only one genomically normal spermatozoon is needed to fertilize one oocyte. A salient difference between natural and ICSI fertilization is that, in the latter, the sperm plasma membrane as well as acrosome (which contains a spectrum of powerful hydrolyzing enzymes) are introduced into an oocyte. For species with small acrosomes, injection of the acrosome into an oocyte apparently does not produce serious problems, but for species like the hamster, with very large acrosomes, injection inevitably results in death of the oocyte (3). We had demonstrated that the contents of the acrosome are potentially harmful to oocytes (4). A notable difference between normal and ICSI fertilization is that repetitive transient increases in intracellular Ca 2ϩ concentration of the oocyte (Ca 2ϩ oscillations), the pivotal signal for oocyte activation (5-8), begins much more slowly in ICSI oocytes than in normally fertilized oocytes. In the mouse, for instance, Ca 2ϩ oscillations begin 1-3 min after plasma membrane fusion between a fertilizing spermatozoon and an oocyte (9), whereas oscillation begins 15-30 min after ICSI (10, 11). In human oocytes, Ca 2ϩ oscillations start 4-12 h after ICSI, when a plasma membrane-intact spermatozoon is injected after immobilization by touching the terminal part of the tail (12). Ca 2ϩ oscillations begin faster (14 Ϯ 6 min) when a spermatozoon is immobilized by applying several piezo pulses to the proximal one-third of the sperm tail before injection (13). Kasai et al. (14) reported that oocyte activation, assessed by the completion of meiosis, occurred earlier when spermatozoa were freed from the plasma membrane before ICSI. Increased fertilization rates aft...

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“…Additionally, epigenetic factors related to early paternal effects on embryo development have been reported. These include factors such as phospholipase C-ζ(PLCζ), which are responsible for regulating calcium oscillations necessary for oocyte activation, but their mechanisms of action are not clearly understood (15). It has been shown that mouse oocyte calcium oscillations are promoted in the presence of PLCζ and are depleted in its absence (15).…”

Section: Discussionmentioning

confidence: 99%

“…These include factors such as phospholipase C-ζ(PLCζ), which are responsible for regulating calcium oscillations necessary for oocyte activation, but their mechanisms of action are not clearly understood (15). It has been shown that mouse oocyte calcium oscillations are promoted in the presence of PLCζ and are depleted in its absence (15). Furthermore, the sperm derived centrosome was shown to be the only functionally active centrosome in the early stages of embryogenesis.…”

Section: Discussionmentioning

confidence: 99%

The effects of sperm quality on embryo development after intracytoplasmic sperm injection

Loutradi

Tarlatzis

Goulis

et al. 2006

J Assist Reprod Genet

117

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Purpose:To explore the possible relationship between sperm quality and embryo development, pregnancy and implantation rates, in patients undergoing intracytoplasmic sperm injection (ICSI). Methods: Fertilization and cleavage rates, quality of embryos, blastocyst development, pregnancy and implantation rates were analyzed in 1020 embryos from 219 couples undergoing first ICSI treatment cycle. The couples were allocated in five groups, according to semen parameters: Group 1: patients with normal semen parameters, Group 2: patients with mild oligoastheno-teratozoospermia, Group 3: patients with severe oligo-astheno-teratozoospermia, Group 4: patients with obstructive azoospermia, Group 5: patients with non-obstructive azoospermia. Results: Fertilization and cleavage rates, quality of embryos as well as blastocyst development rates were significantly reduced, as semen quality decreased. However, no significant differences were observed in clinical pregnancy and implantation rates. Conclusion: Overall, a negative relationship was observed between semen quality and embryo development, even before activation of the embryonic genome, suggesting that sperm can affect embryogenesis from a very early stage.

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The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCζ

Cited by 154 publications

References 62 publications

Phospholipase C-zeta deficiency as a cause for repetitive oocyte fertilization failure during ovarian stimulation for in vitro fertilization with ICSI: a case report

Phospholipase C-zeta deficiency as a cause for repetitive oocyte fertilization failure during ovarian stimulation for in vitro fertilization with ICSI: a case report

Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development

The effects of sperm quality on embryo development after intracytoplasmic sperm injection

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