Patterns of Intracellular Calcium Oscillations in Horse Oocytes Fertilized by Intracytoplasmic Sperm Injection: Possible Explanations for the Low Success of This Assisted Reproduction Technique in the Horse1

Bedford, Sylvia J.; Kurokawa, Manabu; Hinrichs, Katrin; Fissore, Rafael A.

doi:10.1095/biolreprod.103.021485

Cited by 24 publications

(21 citation statements)

References 43 publications

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“…Nonetheless, polyspermic ICSI did not fully re-establish the oscillatory pattern, nor did any of the chemical treatments intended to facilitate the release of the factor. Moreover, our previous results in horse oocytes, which failed to initiate [Ca 2+ ] i oscillations after ICSI but did so immediately after fusing to a mouse MII oocyte, suggest the successful delivery of the sperm factor into the ooplasm (Bedford et al 2004). Hence, these results raise the possibility that the function and/or activation of the sperm factor after release may also be compromised after ICSI, thereby leading to incomplete [Ca 2+ ] i responses.…”

Section: Discussionmentioning

confidence: 71%

Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation

Malcuit

Maserati²,

Takahashi

et al. 2006

Reprod. Fertil. Dev.

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Abstract. Fertilisation by intracytoplasmic sperm injection (ICSI), a technique that bypasses the membrane fusion of the gametes, has been widely used to produce offspring in humans and mice. Success with this technique has lent support to the hypothesis that in mammalian fertilisation, a factor from the sperm, the so-called sperm factor, is responsible for oocyte activation and that the fusion process is not involved in the generation of the hallmark [Ca 2+ ] i signalling seen following fertilisation. However, the success of ICSI has largely eluded large domestic species, such as the bovine, porcine and equine, casting doubt on the current model of oocyte activation at fertilisation in these species. Using Ca 2+ imagery and a series of treatments to manipulate the chemical structure of the sperm, we have investigated the early events of oocyte activation in response to ICSI in the bovine. Our results demonstrate, for the first time, that following ICSI, the majority of bovine oocytes are unable to mount [Ca 2+ ] i oscillations, although, in few cases, the initiation of [Ca 2+ ] i oscillations can occur in a manner indistinguishable from in vitro fertilisation. We also show that bull sperm possess a full complement of sperm factor. However, either the release and/or activation of the sperm factor are compromised after ICSI, leading to the delivery of a defective Ca 2+ stimulus, which results in premature termination of embryo development.

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Section: Discussionmentioning

confidence: 71%

Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation

Malcuit

Maserati²,

Takahashi

et al. 2006

Reprod. Fertil. Dev.

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“…This situation is close to normal fertilization in which SOAF comes into an immediate contact with the ooplasm upon sperm-oocyte membrane fusion. One of the reasons why development of embryos after ICSI has not been very successful in many animal species (2) could be delayed, erratic, or failed Ca 2ϩ oscillations as recorded in bovine and equine oocytes after ICSI (26,27), likely because of a delayed Experiment (Exp.) A, a motile spermatozoon with intact head and tail was injected into each oocyte; B, only the head was injected after separation of the head and tail by piezo pulses; C and E, spermatozoa were individually treated for 1 min with 0.02% LL or 0.02% Triton X-100 and washed in Hepes-CZB containing 12% PVP for 1 min before injection of a single sperm head isolated from the tail by piezo pulses; D and F, Ϸ10 5 spermatozoa were treated for 1 min with 0.02% LL or 0.02% Triton X-100, washed by centrifugation for 3 min, and left in Hepes-CZB for 5-60 min before injection of a single sperm head isolated from the tail by piezo pulses.…”

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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“…In experiment 1, the second ionomycin treatment was performed 2 h after the first to provide two large amplitude calcium spikes within the normal period in which calcium oscillates in the horse oocyte after injection of sperm (120 min; Bedford et al 2003). Ionomycin treatment in the SECI group was performed 20 min after sperm extract injection to provide a large amplitude spike at the typical interval of oscillation after sperm extract injection (10-30 min; Bedford et al 2003Bedford et al , 2004. In experiment 2, the effect of ionomycin treatment before or after sperm extract injection was evaluated to determine the effect of the timing of the calcium spike in relation to oscillations induced by sperm extract injection; the time between the two ionomycin treatments in the 2!I group was changed to 20 min to duplicate the timing between ionomycin and sperm extract injections in the other treatments in this experiment.…”

Section: Discussionmentioning

confidence: 99%

Production of cloned horse foals using roscovitine-treated donor cells and activation with sperm extract and/or ionomycin

Hinrichs

Choi²,

Varner³

et al. 2007

Reproduction

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We evaluated the effect of different activation treatments on the production of blastocysts and foals by nuclear transfer. Donor cells were prepared using roscovitine treatment, which has previously been associated with increased production of viable offspring. All activation treatments were followed by culture in 6-dimethylaminopurine (6-DMAP) for 4 h. In experiment 1, blastocyst production after activation by injection of sperm extract followed by treatment with ionomycin was significantly higher than that for activation with a serial treatment of ionomycin, 6-DMAP, and ionomycin (12.5 vs 2.8%; P!0.05) and tended to be higher than that for injection of sperm extract alone (3.4%; PZ0.07). In experiment 2, there were no significant differences in blastocyst development among treatments with ionomycin once or twice, sperm extract then ionomycin, or ionomycin then sperm extract (range 4.6-7.3%). Overall, transfer of 26 blastocysts resulted in 16 pregnancies (62%) and 9 live foals (35% of transferred embryos). Treatment with sperm extract followed by ionomycin produced a live foal rate per embryo transferred of 5/10 (50%). One foal died of pneumonia 48 h post partum and one foal died at 1 week of age after complications during induction of anesthesia; the remaining seven foals are currently 10-14 months of age.

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Patterns of Intracellular Calcium Oscillations in Horse Oocytes Fertilized by Intracytoplasmic Sperm Injection: Possible Explanations for the Low Success of This Assisted Reproduction Technique in the Horse1

Cited by 24 publications

References 43 publications

Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation

Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation

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

Production of cloned horse foals using roscovitine-treated donor cells and activation with sperm extract and/or ionomycin

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