Oocyte maturation, follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting

Gook, Debra A.; Edgar, David; Borg, Jessica; Archer, J.; Lutjen, P.; McBain, John

doi:10.1093/humrep/deg365

Cited by 106 publications

(52 citation statements)

References 52 publications

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“…Likewise, only few human antral follicles developed from primordial follicles after xeno-transplantation into immune-deficient mice (32). One case of successful ovarian transplantation between monozygotic twins discordant for premature ovarian failure has been reported, and the patient delivered a healthy baby (33).…”

Section: Discussionmentioning

confidence: 99%

Activation of dormant ovarian follicles to generate mature eggs

Kawamura

Cheng

et al. 2010

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

375

340

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Although multiple follicles are present in mammalian ovaries, most of them remain dormant for years or decades. During reproductive life, some follicles are activated for development. Genetically modified mouse models with oocyte-specific deletion of genes in the PTEN-PI3K-Akt-Foxo3 pathway exhibited premature activation of all dormant follicles. Using an inhibitor of the Phosphatase with TENsin homology deleted in chromosome 10 (PTEN) phosphatase and a PI3K activating peptide, we found that short-term treatment of neonatal mouse ovaries increased nuclear exclusion of Foxo3 in primordial oocytes. After transplantation under kidney capsules of ovariectomized hosts, treated follicles developed to the preovulatory stage with mature eggs displaying normal epigenetic changes of imprinted genes. After in vitro fertilization and embryo transfer, healthy progeny with proven fertility were delivered. Human ovarian cortical fragments from cancer patients were also treated with the PTEN inhibitor. After xeno-transplantation to immune-deficient mice for 6 months, primordial follicles developed to the preovulatory stage with oocytes capable of undergoing nuclear maturation. Major differences between male and female mammals are unlimited number of sperm and paucity of mature oocytes. Thus, short-term in vitro activation of dormant ovarian follicles after stimulation of the PI3K-Akt pathway allows the generation of a large supply of mature female germ cells for future treatment of infertile women with a diminishing ovarian reserve and for cancer patients with cryo-preserved ovaries. Generation of a large number of human oocytes also facilitates future derivation of embryonic stem cells for regenerative medicine.

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Section: Discussionmentioning

confidence: 99%

Activation of dormant ovarian follicles to generate mature eggs

Kawamura

Cheng

et al. 2010

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

375

340

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“…Snow et al (2002) demonstrated that oocytes that grow within mouse ovarian tissue xenografted to nude rats acquire the ability to generate pups. Ovarian tissues have been prepared from species phylogenetically distant from mice, including humans (Oktay et al 1998, Weissman et al 1999, Kim et al 2002, Gook et al 2003, dogs (Metcalfe et al 2001), monkeys (Candy et al 1995), sheep (Gosden et al 1994), cows (Senbon et al 2003), pigs (Kaneko et al 2003, Kagawa et al 2005, tammar wallaby (Mattiske et al 2002) and common wombats (Cleary et al 2003(Cleary et al , 2004, and xenografted to immunodeficient mice. To our knowledge, only one study (Kaneko et al 2003), in which neonatal pig ovarian tissues were xenografted, has proven that primordial oocytes can develop in the host mice and acquire fertilizing ability in vitro.…”

Section: Introductionmentioning

confidence: 99%

“…Cleary et al (2003) indicated that greater numbers of morphologically normal oocytes were recovered from ovarian grafts of common wombats after the host mice were given follicle-stimulating hormone (FSH) for 4 or 7 days. Treatment of host mice with FSH for over 20 weeks (Gook et al 2003), equine chorionic gonadotrophin (eCG) for 4 weeks (Kim et al 2002) or human menopausal gonadotrophin (hMG) for 14 days (Weissman et al 1999) increased the number of antral follicles within human ovarian xenografts, and the former two studies showed that some antral follicles formed early corpora lutea in response to human chorionic gonadotrophin (hCG; Kim et al 2002, Gook et al 2003 with resumption of meiosis of the oocytes (Gook et al 2003). We previously optimized the timing of eCG treatment of host mice in terms of follicular growth and oocyte recovery, and found that more oocytes with fertilizing ability were collected from antral follicles when eCG was given 60 days after estrus was first detected in the host mice (Kaneko et al 2003).…”

Section: Introductionmentioning

confidence: 99%

Effects of gonadotrophin treatments on meiotic and developmental competence of oocytes in porcine primordial follicles following xenografting to nude mice

Kaneko¹,

Kikuchi²,

Noguchi³

et al. 2006

Reproduction

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Our objective was to improve the developmental ability of oocytes in porcine primordial follicles xenografted to nude mice, by treating the host mice with gonadotrophins to accelerate follicular growth. Ovarian tissues from 20-day-old piglets, in which most of the follicles were primordial, were transplanted under the kidney capsules of ovariectomized nude mice. Gonadotrophin treatments were commenced around 60 days after vaginal cornification in the mice. Ovarian grafts were obtained 2 or 3 days after treatment with equine chorionic gonadotrophin (eCG-2 and eCG-3 groups), after porcine FSH infusion for 7 or 14 days, or after infusion of porcine FSH for 14 days with a single injection of estradiol antiserum (FSH-7, FSH-14 and FSH-14EA groups, respectively). Gonadotrophin treatments accelerated follicular growth within the xenografts compared with that in control mice given no gonadotrophins, consistent with higher (P < 0.05) circulating inhibin levels in the gonadotrophin-treated mice. In contrast, circulating mouse FSH levels were significantly (P < 0.05) depressed. We recovered large numbers of full-sized oocytes with meiotic competence to the mature stage from the eCG-3, FSH-7, and FSH-14EA, unlike in the control group. Moreover, 56% of matured oocytes with the first polar body (n 5 39) were fertilized in vitro in the FSH-14EA group. After in vitro fertilization and subsequent culture for 7 days, one blastocyst was obtained from each of the eCG-3, FSH-7 and, FSH-14EA groups, whereas no blastocysts appeared in the other groups. Exogenous gonadotrophinsnot mouse FSH -stimulated the growing follicles that had developed from the primordial follicles in the xenografts: the effects were incomplete but improved to some extent the meiotic and developmental abilities of the oocytes.

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“…Harvesting of ovarian tissue via laparoscopic surgery can be performed at any time during the menstrual cycle. Furthermore, the removal and appropriate cryopreservation of a small area of ovary containing an abundance of primordial follicles has more theoretical potential for future fertility than cryopreserved oocytes (Gook et al, 1999(Gook et al, , 2003. This tissue can then be reimplanted either orthotopically (Radford et al,2001;Meirow et al, 2005), or heterotopically (Donnez et al, 2004;Oktay et al, 2004;Wolner-Hanssen et al, 2005), with the demonstrated capacity to restore both endocrine function and fertility (Donnez et al, 2004;Meirow et al, 2005).…”

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confidence: 99%

Lack of evidence of disease contamination in ovarian tissue harvested for cryopreservation from patients with Hodgkin lymphoma and analysis of factors predictive of oocyte yield

et al. 2006

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Ovarian cryopreservation is a promising technique to preserve fertility in women with Hodgkin lymphoma (HL) treated with chemotherapy. Thus, the aim of this study was to examine harvested ovarian tissue for subclinical involvement by HL by morphology/ immunohistochemistry, and to define patient and treatment factors predictive of oocyte yield. This was a retrospective analysis of 26 ovarian tissue samples harvested for cryopreservation from women with HL. Histology, immunohistochemistry and follicle density (number mm À3 ) was examined. Disease status and preharvest chemotherapy details were obtained on 24 patients. The median age was 22 years (range 13 -29). Seven of 24 patients had infradiaphragmatic disease at time of harvest. Nine of 20 patients had received chemotherapy preharvest (ABVD (Adriamycin s , Bleomycin, Vinblastine and Dacarbazine) ¼ 7, other regimens ¼ 2). The seven receiving ABVD showed no difference in follicle density compared to patients not receiving treatment (n ¼ 14); (median ¼ 1555 vs 1620 mm 3 P ¼ 0.97). Follicle density measurement showed no correlation with patient age (R 2 ¼ 0.0001, P ¼ 0.99). There was no evidence of HL involvement in the 26 samples examined (95% CI ¼ 0 -11%). In conclusion, subclinical involvement of HL has not been identified in ovarian tissue, even when patients have infradiaphragmatic disease. Furthermore, the quality of tissue harvested does not appear to be adversely affected by patient's age or prior ABVD chemotherapy.

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Oocyte maturation, follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting

Abstract: Follicles cryopreserved within human ovarian tissue using the PROH procedure, can develop to the antral stage and undergo periovulatory changes following xenografting and exposure to a luteinizing stimulus.

Cited by 106 publications

References 52 publications

Activation of dormant ovarian follicles to generate mature eggs

Activation of dormant ovarian follicles to generate mature eggs

Effects of gonadotrophin treatments on meiotic and developmental competence of oocytes in porcine primordial follicles following xenografting to nude mice

Lack of evidence of disease contamination in ovarian tissue harvested for cryopreservation from patients with Hodgkin lymphoma and analysis of factors predictive of oocyte yield

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