In vitro growth and steroidogenesis of dog follicles are influenced by the physical and hormonal microenvironment

Songsasen, Nucharin; Woodruff, Teresa K.; Wildt, David E.

doi:10.1530/rep-10-0442

Cited by 51 publications

(46 citation statements)

References 78 publications

(144 reference statements)

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“…With the ultimate goal of translating eIVFG to young females with any fertility threatening condition, tremendous advances have been made in supporting follicle growth and oocyte development in large mammalian species such as domestic dogs, baboons, rhesus monkeys, and humans (Xu et al 2009a, Xu et al 2009b, Xu et al 2010, Songsasen et al 2011, Xu et al 2011a, Xu et al 2011b). Rhesus monkey secondary follicles have been cultured in vitro , produced MII oocytes, and cleaved to two-cell stage embryos and arrested with uneven cleavage after IVF (Xu et al 2011a).…”

Section: Discussionmentioning

confidence: 99%

“…This method is significant because it provides a potential alternative to ovarian tissue transplantation for preserving fertility and does not have the inherent risk of reintroducing cancer cells because follicles develop completely in vitro (Woodruff 2007). Encapsulated in vitro follicle growth (eIVFG) has successfully resulted in live births in mice (Xu et al 2006a) in addition to follicle growth, oocyte development, and preimplantation embryo development in other large mammalian species (Xu et al 2009a, Xu et al 2009b, Xu et al 2010, Songsasen et al 2011, Xu et al 2011a). Thus, eIVFG is among one of several other systems that has been successful in supporting the in vitro growth and development of ovarian follicles (Smitz et al 2010, Telfer & McLaughlin 2012).…”

Section: Introductionmentioning

confidence: 99%

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Size-specific follicle selection improves mouse oocyte reproductive outcomes

Xiao¹,

Duncan

Bai³

et al. 2015

Reproduction

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Encapsulated in vitro follicle growth (eIVFG) has great potential to provide an additional fertility preservation option for young women and girls with cancer or other reproductive health threatening diseases. Currently, follicles are cultured for a defined period of time and analyzed as a cohort. However, follicle growth is not synchronous, and culturing follicles for insufficient or excessive times can result in compromised gamete quality. Our objective is to determine whether the selection of follicles based on size, rather than absolute culture time, better predict follicle maturity and oocyte quality. Multilayer secondary mouse follicles were isolated and encapsulated in 0.25% alginate. Follicles were cultured individually either for defined time periods or up to specific follicle diameter ranges, at which point several reproductive endpoints were analyzed. The metaphase II (MII) percentage after oocyte maturation on day 6 was the highest (85%) when follicles were cultured for specific days. However, if follicles were cultured to a terminal diameter of 300–350 μm irrespective of absolute time in culture, 93% of the oocytes reached MII. More than 90% of MII oocytes matured from follicles with diameters of 300–350 μm showed normal spindle morphology and chromosome alignment, 85% of oocytes showed 2 pronuclei after in vitro fertilization (IVF), 81% developed into the 2-cell embryo stage, and 38% developed to the blastocyst stage, all significantly higher than the percentages in the other follicle size groups. Our study demonstrates that size-specific follicle selection can be used as a non-invasive marker to identify high quality oocytes and improve reproductive outcomes during eIVFG.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Size-specific follicle selection improves mouse oocyte reproductive outcomes

Xiao¹,

Duncan

Bai³

et al. 2015

Reproduction

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“…The alginate hydrogel culture system sustained growth and steroidogenesis of pre- and early-antral dog follicles for 10 days (71). Further development of this culture system may contribute to the conservation of a growing list of wild canid species threatened in nature.…”

Section: Follicle Culture System Applicationsmentioning

confidence: 99%

Bioengineering the Ovarian Follicle Microenvironment

Shea

Woodruff

Shikanov

2014

Annu. Rev. Biomed. Eng.

150

108

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Chemo- and radiation therapies used to treat cancer can have the unintended effect of making patients infertile. Clinically established fertility preservation methods, such as egg and embryo cryopreservation, are not applicable to all patients, which has motivated the development of strategies that involve ovarian tissue removal and cryopreservation before the first sterilizing treatment. To restore fertility at a later date, the early-stage follicles present in the tissue must be matured to produce functional oocytes, a process that is not possible using existing cell culture technologies. This review describes the application of tissue engineering principles to promote ovarian follicle maturation and produce mature oocytes through either in vitro culture or transplantation. The design principles for these engineered systems are presented, along with identification of emerging opportunities in reproductive biology.

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“…We developed an encapsulated in vitro follicle growth (eIVFG) culture system, which preserves 3D follicular structure with paracrine signaling maintained between oocyte, granulosa and theca cells (Kreeger et al, 2006;Tingen et al, 2011;Tagler et al, 2012;Hornick et al, 2013). In addition to murine follicles, success to date in the culture of larger mammalian species has been reported in the alginate system including follicles from dog, rhesus macaque, goat, baboon and human (Xu et al, 2009a(Xu et al, ,b, 2010(Xu et al, , 2011b(Xu et al, ,c, 2013aSongsasen et al, 2011;Camboni et al, 2013;Fisher et al, 2013;Araujo et al, 2014;Silva et al, 2014;Wang et al, 2014). Further, eIVFG has facilitated studies of inter-and intra-follicular mechanisms governing follicularphase processes including antrum formation, oocyte maturation and granulosa cell proliferation (Kreeger et al, 2006;West-Farrell et al, 2009;Hornick et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Engineering the ovarian cycle using in vitro follicle culture

et al. 2015

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study question: Can cultured follicles model the ovarian cycle, including follicular-and luteal-phase hormone synthesis patterns and ovulation?summary answer: Under gonadotrophin stimulation, murine follicles grown in an encapsulated three-dimensional system ovulate in vitro and murine and human follicle hormone synthesis mimics follicular and luteal phases expected in vivo.what is known already: Studies of the human ovary and follicle function are limited by the availability of human tissue and lack of in vitro models. We developed an encapsulated in vitro follicle growth (eIVFG) culture system, which preserves 3D follicular structure. Thus far, the alginate system has supported the culture of follicles from mice, dog, rhesus macaque, baboon and human. These studies have shown that cultured follicles synthesize steroid hormones similar to those observed during the follicular phase in vivo. study design, size, duration: Cultured murine follicles were treated with human chorionic gonadotrophin (hCG) and epidermal growth factor (EGF) and either assayed for luteinization or removed from alginate beads and assayed for ovulation. Human follicles were also cultured, treated with follicle-stimulating hormone (FSH), hCG and EGF to mimic gonadotrophin changes throughout the ovarian cycle, and culture medium was assayed for hormone production.participants/materials, setting, methods: Murine and human follicles were cultured in alginate hydrogel and hormone production [17b-estradiol, progesterone, inhibin A, inhibin B, activin A and anti-Müllerian hormone (AMH)] was quantified in medium by enzyme-linked immuno assay (ELISA). Human ovarian tissue was acquired from females between 6 and 34 years of age with a cancer diagnosis. These participants were undergoing ovarian tissue cryopreservation at National Physicians Cooperative sites as part of the Oncofertility Consortium.main results and the role of chance: When grown in this system, 96% of mouse follicles ovulated in response to hCG and released meiotically competent eggs. Ovulated follicles recapitulated transcriptional, morphologic and hormone synthesis patterns post-luteinizing hormone (LH/hCG). In addition to rodent follicles, individual human follicles secreted steroid and peptide hormones that mimicked the patterns of serum hormones observed during the menstrual cycle.limitations, reasons for caution: This was a descriptive study of an in vitro model of ovulation and the ovarian hormone cycle.The ovulation studies were limited to murine tissue and further studies are needed to optimize conditions using other species.wider implications of the findings: The eIVFG system reliably phenocopies the in vivo ovarian cycle and provides a new tool to study human follicle biology and the influence of cycling female hormones on other tissue systems in vitro. study funding/competing interest(s): This work was supported by NIH U54 HD041857, NIH U54 HD076188, NIH UH2 E5022920, NIH UH3 TR001207 and F30 AG040916 (R.M.S.). The content is solely the responsibility of the authors and do...

show abstract

In vitro growth and steroidogenesis of dog follicles are influenced by the physical and hormonal microenvironment

Cited by 51 publications

References 78 publications

Size-specific follicle selection improves mouse oocyte reproductive outcomes

Size-specific follicle selection improves mouse oocyte reproductive outcomes

Bioengineering the Ovarian Follicle Microenvironment

Engineering the ovarian cycle using in vitro follicle culture

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