Offspring from oocytes grown in frozen-thawed ovarian tissues transplanted to male and female bodies : Reproductive and Developmental Medicine

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Original Article

Offspring from oocytes grown in frozen-thawed ovarian tissues transplanted to male and female bodies

Yan, Jie1; Cai, Yu-Fang2; Dai, Shan-Jun3; He, Xiao-Jin4; Sun, Ying-Pu3; Cao, Yun-Xia4; Qiao, Jie1; Chian, Ri-Cheng5,*

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Reproductive and Developmental Medicine: March 2022 - Volume 6 - Issue 1 - p 13-19
doi: 10.1097/RD9.0000000000000005
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Abstract

Introduction

The first attempt to ovarian tissue transplantation (OTT) was done over a century ago[1,2]. The initial purpose of OTT was to cure premature ovarian failure (POF) and infertility and was then considered as an alternative to hormone replacement therapy[3]. Recently, OTT became an increasingly popular strategy for female fertility preservation for children and young women with cancer due to the alternative treatment of gonadotoxic cancer treatments with chemotherapy and/or radiation causing a potential long-term side effect with POF[4]. There are few options available for female fertility preservation before cancer treatments; one of these options being ovarian tissue cryopreservation[5,6].

The frozen-thawed ovarian tissue can be used to perform a relative long period of culture in vitro for follicular growth but with limited success[7-12]. Another alternative is OTT, which can result in live births, especially in humans[13,14] and widely applied to cancer patients for fertility preservation before chemotherapy, radiotherapy treatments and/or surgery. It has been reported that orthotopic transplantation helped more than 50% of women to conceive naturally[15], therefore it has been considered that ovarian tissue cryopreservation has a low usage rate and high live-birth rate after transplantation[16].

Sometimes, an orthotopic site may not be appropriate for OTT. Therefore, heterotopic transplantation of ovarian tissue can be an option. Endocrine function recovery has been described consistently after heterotopic ovarian transplantation[17,18]. Interestingly, human ovarian tissue xenografted to male mice contains morphologically normal follicles and possesses more pre-antral and antral follicles after stimulation with human menopausal gonadotrophin (hMG)[19]. Hormonal environment of male mice can support the growth of oocytes in fresh ovarian allografts under the kidney capsules and these oocytes can produce live offspring[20]. However, there are very few successes of the heterotopic transplantation of frozen-thawed ovarian tissue[21-23]. Unlike orthotopic transplantation, in vitro fertilization procedure is required after heterotopic transplantation of ovarian tissues for conception.

We show that a normal mouse offspring can be produced from the oocytes grown in frozen-thawed ovarian tissue transplanted subcutaneously to male mouse body. We found that there is no difference in follicle development in both fresh and frozen-thawed ovarian tissue following heterotopic transplantation to nude severe combined immunodeficiency (SCID) adult male mice without castrating. The fully grown immature oocytes from the ovarian tissues were natured, fertilized and developed to blastocyst stage in vitro. Following the transfer of the resulted embryos, the obtained offspring was healthy and fertile.

Materials and methods

Cluster of differentiation 1 (CD1) mice (6-8 weeks) were used in this study as ovarian tissue donor and foster mother for embryo transfer. Sperm from CD1 male mice were used for intracytoplasmic sperm injection (ICSI). Nude SCID mice (8 weeks) were used as the recipient of OTT.

Ovarian tissue freezing and thawing

The obtained whole ovary is cut in 4 equal pieces for freezing (approximately 1.5 mm × 1.5 mm × 1.5 mm). The ovarian tissues are suspended in equilibration solution containing 7.5% ethylene glycol (EG) and 1,2-propanediol (PROH) for 30 minutes at room temperature, and the ovarian tissues are then transferred in vitrification solution containing 15% EG + PROH and 0.5 mol/L sucrose for 10 minutes. Ovarian tissues are then loaded on a device, McGill Cryoleaf, and plunged into liquid nitrogen directly for storage. For thawing, the ovarian tissues are inserted directly into 37°C thawing solution containing 1.0 mol/L sucrose for 5 minutes. The thawed ovarian tissues are transferred to 0.5 mol/L to 0.25 mol/L sucrose solutions for 10 minutes, respectively, and washed twice with 4-(2-hydroxyethyl)-1-plperazineethanesulfonic acid (HEPES)-buffered culture medium[24] for 20 minutes at room temperature and incubated at 37 °C before transplantation.

Ovarian tissue transplantation and collection

The frozen-thawed ovarian tissues are transferred to 4 sites on each mouse (both female and male) subcutaneously. Under anaesthesia, a skin hole is cut at neck-back and waist-back respectively, and the frozen-thawed ovarian tissues are inserted to both side under skin through the hole. The incision on skin is sewn up. After 3 months, the female and male mice are injected with 5.0 IU pregnant mare gonadotropin (PMSG) intraperitoneally. Post 48 hours of injection, the mouse is then killed for ovarian transplant collection.

Histological observation

The ovarian tissues are fixed for 24 hours at 4°C in 4% formaldehyde in phosphate-buffered saline (pH 7.4), and dehydrated, paraffin embedded for section. The sections are stained with haematoxylin and eosin and then the sections are observed under light microscope.

Oocyte maturation in vitro

Only fully grown oocytes with contacted cumulus cells (cumulus-oocyte complexes, COCs) are selected for maturation in culture. COCs are cultured with 1 mL of Oocyte Maturation Medium[24] containing 75 mIU/mL Follicle-stimulating hormone (FSH) and Luteinizing hormone (LH) for 16 to 18 hours in 5% CO2 incubator with high humidity at 37 °C.

Fertilization and embryo culture in vitro

In vitro matured oocytes are inseminated with fresh sperm by ICSI using piezo-pulse system[25]. After ICSI, oocytes are transferred to Embryo Maintenance Medium for further culture for 5 days. The developed blastocysts are frozen using the vitrification method[26-28] and stored in liquid nitrogen (-196 °C) tank until embryo transfer.

Embryo thawing and transfer

The frozen blastocysts are thawed as described[27,28]. After thawing, the thawed blastocysts are incubated for at least 2 hours before transfer. The foster mice mothers had been mated with vasectomised male 3 days prior. Live birth is monitored at 19 days after embryo transfer and the offspring is raised for fertility test.

Results

As shown in Table 1, we initially transplanted both frozen-thawed and fresh ovarian tissues to female nude SCID adult mice without any ovariectomizing. We were able to collect the transplants after 3 months of transplantation and isolate fully grown immature oocytes from both frozen-thawed and fresh transplanted ovarian tissues. The collected immature oocytes are matured in vitro, fertilized by ICSI, and developed to blastocyst stage in vitro (Table 2). Thus, the experiments are set in order to determine if the follicles are able to survive and develop in the transplants when they are transplanted to male nude SCID adult mice.

Table 1 - Immature oocytes collected from the transplanted ovarian tissues with or without freezing and matured in vitro.

Gender of recipients for ovarian tissue transplantation

Ovarian tissues with (+) or without (-) freezing

No. of recipients

No. of ovarian tissues transferred

No. of ovarian tissues recovered (%)*

No. of immature oocytes selected (mean ± SD)*

No. of oocytes matured in vitro (%)*

Female

+

27

108

79 (73.1)

124 (1.5 ± 1.1)

124 (100.0)

Female

-

19

76

65 (85.5)

89 (1.4±1.4)

89 (100.0)

* There is no significant difference between 2 groups. Data were analysed using the χ2 test.

Table 2 - Embryonic development of in vitro matured oocytes collected from the transplanted ovarian tissues with or without freezing followed by intracytoplasmic injection (ICSI)

Gender of recipients for ovarian tissue transplantation

Ovarian tissue with (+) or without (-) freezing

No. of eggs survived post-ICSI

No. of eggs cleaved (%)*

No. of blastocysts developed (%)*

Female

+

62

55 (88.7)

6 (9.7)

Female

-

63

53 (84.1)

11 (17.9)

* There is no significant difference between 2 groups. Data were analyzed using the χ2 test.

Four pieces of frozen-thawed ovarian tissues are transplanted subcutaneously to different sites on a male nude SCID adult mouse as a recipient (Fig. 1, A). As control, the fresh ovarian tissues are also transplanted accordingly. After transplantation, the transplants are collected at different times for histological observation to confirm whether there is any survival and developmental of follicles. Interestingly, the follicles developed in the transplanted ovarian tissues (Fig. 1, B and C). We decided to inject 5 IU of PMSG intraperitoneally before the harvesting of immature oocytes. Post 48 hours of PMSG injection, the ovarian tissues are collected from the transplanted sites (Fig. 1, D and E). We were able to collect the transplanted ovarian tissues with relatively high recovery rate in both frozen-thawed and fresh ovarian tissue transplants (Table 3). The collected subcutaneous transplant pockets (Fig. 1, F) are transferred to a Petri dish containing medium for immature oocytes retrieval (Fig. 1, G).

F1
Fig. 1.:
Transplantation and collection of ovarian tissues from male mice. (A) Ovarian tissues were transplanted to 4 different sites (red circles) at the back of a nude SCID adult mouse. (B) Histological observation of the transplanted fresh ovarian tissue collected after 3 months of transplantation. (C) Histological observation of the transplanted frozen-thawed ovarian tissue collected after 3 months of transplantation. There were many pre-antral follicles observed in both transplants. (D) Ovarian tissue transplant was under neck-back after PMSG injection at collection. Arrow indicates blood vessels connected to the ovarian tissue. (E) Ovarian tissue transplant was under waist-back after PMSG injection at collection. Arrow indicates antral follicle developed on the surface of ovarian tissue transplant. (F) Ovarian tissue transplant (subcutaneous packet) was collected a forceps. (G) Fresh (left) and frozen-thawed (right) ovarian tissue transplants were collected from male mice for egg retrieval.
Table 3 - Immature oocytes collected from the transplanted ovarian tissues with or without freezing and matured in vitro.

Gender of recipients for ovarian tissue transplantation

Ovarian tissues with (+) or without (-) freezing

No. of recipients

No. of ovarian tissues transferred

No. of ovarian tissues recovered (%)*

No. of immature oocytes selected (mean ± SD)*

No. of oocytes matured in vitro (%)*

Male

+

73

292

234 (80.1)

383 (1.6 ± 1.2)

373 (97.3)

Male

-

65

260

218 (83.9)

330 (1.5 ± 1.1)

316 (95.8)

* There is no significant difference between 2 groups. Data were analysed using the χ2 test.

The visual follicles are punctured with a small needle and the fully grown immature oocytes are selected for in vitro maturation culture (Fig. 2, A). The fully grown immature oocytes become mature in vitro to metaphase-II stage following culture for 16 hours in maturation medium. The matured oocytes (Fig. 2, B) are inseminated by ICSI, and the fertilized zygotes undergo cleavage. Following culture of the cleaved embryos for 5 days, the embryos developed to blastocyst stage (Fig. 2, C). The produced blastocysts from both frozen-thawed and fresh ovarian tissues are frozen using the vitrification method and stored at -196°C for at least 3 months. We do not find any differences between the frozen-thawed and fresh ovarian transplants in term of oocyte quality, cleavage, and embryo development to blastocyst rates (Table 4).

F2
Fig. 2.:
Offspring from the eggs grown in the transplanted ovarian tissues. (A) Cumulus-oocyte complexes were collected from transplanted ovarian tissues. (B) Eggs become mature after 16 hours of culture. (C) Embryos developed to blastocyst stage after 5-day culture following ICSI. All blastocysts were frozen with vitrification method and kept in liquid nitrogen before transfer. (D) Blastocysts after thawing. (E) Offspring were produced from the eggs grown in transplanted ovarian tissues. Left and right photos indicate the first 2 mice that delivered 6 and 4 pups, respectively. (F) A photo of offspring at 6 weeks. Scale bars for A-D, 50 μm.
Table 4 - Embryonic development and live births from the oocytes grown in male body

Gender of recipients for ovarian tissue transplantation

Ovarian tissue with (+) or without (-) freezing

No. of oocytes survived post-ICSI

No. of oocytes cleaved (%)*

No. of blastocysts developed (%)*

No. of transferred embryos after thawing (recipients)

No. of newborn from transferred embryos (%)*

Male

+

317

268 (84.5)

75 (28.0)

48 (4)

13 (20.8)

Male

-

279

222 (79.7)

56 (25.2)

48 (4)

12 (25.0)

* There is no significant difference between 2 groups. Data were analysed using the χ2 test.

The frozen blastocysts are thawed (Fig. 2, D) and cultured for 2 hours before transfer. We transferred 14 frozen-thawed blastocysts to each foster mouse, and each group with 4 recipients of foster mice. Post 19-day transfer, 3 foster mothers from the frozen-thawed ovarian tissue transplant group delivered 13 live pups (6, 4, 2, and 1, respectively) and 4 foster mothers from the fresh ovarian tissue transplant group delivered 12 live pups (7, 4,1, and 0, respectively) (Table 4).

The produced offspring were normal in appearance and grew healthy as well as fertile.

Discussion

We demonstrate that healthy live births can be produced from oocytes grown in male body in frozen-thawed ovarian tissues following subcutaneously transplantation. Ovarian tissue freezing is the only option for preserving the fertility of pre-pubertal patients with cancer. Ovarian tissue cryopreservation and transplantation is an important option for fertility preservation in adult patients with cancer who need immediate chemotherapy or do not wish to undergo ovarian stimulation.

More than 50% of primordial follicles and all growing follicles disappeared from ovarian autograft[29], and revascularization of transplanted ovarian tissues required 3 to 7 days after transplantation[30]. The primordial follicles also survive in ovarian allograft for months before immune rejection in different species[31] and observed comparatively slow rejection time of ovarian allograft compared with skin allograft in rat[3,32]. In addition, the primordial follicles survive in ovarian xenograft in nude SCID mice[33,34].

Although autograft[18,35,36] and allograft[37,38] with fresh or frozen-thawed ovarian tissues result in follicular survival and development as well as pregnancies and live births, the exact mechanism of survival and folliculogenesis in the transplanted ovarian tissues seems unclear. Follicular survival and development are observed in xenograft with frozen-thawed ovarian tissues when they are transplanted to nude SCID mice[33,34,39,40]. Folliculogenesis is one of the most complex of processes for cell proliferation and differentiation in female ovary controlled by the reproductive endocrine system and the progression of a number of small primordial follicles develop into large pre-ovulatory follicles.

Live births reported from oocytes grown in transplanted ovarian tissues are in mice[41], rats[42], sheep[34], and humans[13,14]. Most of those live births are from autologous orthotopic transplantation with the exceptions of mouse and monkey, which is after heterotopic transplantation of fresh ovarian tissue[20,43]. So far, there are more than 130 reported live births in the world[5,6]. There are no reported live births from oocytes grown from heterotopic transplantation of frozen-thawed ovarian tissue in any species. We believe it is the first time we are reporting live births from oocytes grown in the male body following frozen-thawed ovarian tissues transplanted subcutaneously, and the obtained offspring was healthy and fertile (data not shown).

In most experiments, allograft and xenograft of ovarian tissues are transplanted to the ovariectomized hosts in order to monitor the fertile potential restore with the changes of steroid levels. It is common belief that the recovery of transplants is faster in ovariectomized hosts[44], although there is no proven evidence yet. Little is known about the mechanism of the follicles and their survival and development in ovarian tissues after transplanting in the male body. Our results confirm indirectly that steroid hormones must work as both endocrine and paracrine factors to control follicular survival and development in the transplanted ovarian tissue.

Androgen, FSH, anti-Müllerian hormone and estradiol are essential in folliculogenesis[45]. Androgen promotes early follicle growth within the primate ovary[46]. Human ovarian tissue xenografted to male mice contains morphologically normal follicles and possesses more pre-antral and antral follicles after stimulation with hMG[19]. Additionally, human[19] and mouse[47] ovarian tissue xenografted to male rodents treated with exogenous gonadotrophins produce more oocytes per graft than grafts to female recipients, indicating that male recipients may be a better model for increasing oocyte yield from ovarian grafts.

The normal hormonal environment can support the production of developmentally competent oocytes[20]. In vitro study demonstrated that androgen and estrogen augment follicle survival and growth in the presence of FSH during culture[48]. Although androgen and estrogen promote follicle survival and growth in vitro in the absence of FSH, their growth-promoting effects are limited to the pre-antral to early antral stage[49]. However, it seems that the exact effect of androgen on follicle survival and growth in the transplanted ovarian tissues is not fully understood yet.

In conclusion, we believe that the success of this experiment in mouse model provides a broad platform of opportunities for the study of mechanism of folliculogenesis and conservation biology. Furthermore, this success may open a potentiality to new clinical application for cryopreserved ovarian tissue.

Acknowledgments

None.

Author contributions

J.Y. and Y.C. performed the experiments; S.D. and X.H. participated in data analysis and interpretation; Y.S., Y.C. and J.Q. supervised the experiments and discussed the manuscript revision; R.C. designed and drafted the manuscript. All authors contributed to the final manuscript and approved the submitted version.

Funding(s)

Financial support and sponsorship: J.Y. was sponsored by Peking University Third Hospital Beijing, China; Y.C. was sponsored by Ningxia Medical College, Yinchuan, China; S.D. was sponsored by The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; X.H. was sponsored by Anhui Medical University, Hefei, China.

Conflicts of interest

All authors declare no conflict of interest.

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Keywords:

Ovarian tissue; Cryopreservation; Transplantation; Oocytes; Live births

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