Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: Effects of gonadotrophins, oxygen and fetuin

Jing Xu, M. S. Lawson, R. R. Yeoman, K. Y. Pau, S. L. Barrett, Mary Zelinski, Richard Stouffer

    Research output: Contribution to journalArticle

    97 Citations (Scopus)

    Abstract

    Background: An alginate-based matrix supports the three-dimensional (3D) architecture of non-human primate follicles and, in the presence of FSH, permits the in vitro development of pre-antral follicles to the small antral stage, including the production of ovarian steroids and paracrine factors. The current study investigated the ability of gonadotrophins, fetuin and oxygen (O 2) to improve primate follicle growth and oocyte maturation in vitro.MethodsMacaque secondary follicles were isolated from the early follicular phase ovaries, encapsulated in a sodium alginate matrix and cultured individually for 40 days in supplemented medium. The effects of recombinant human (rh) FSH (15, 3 and 0.3 ng/ml for high, medium and low FSH, respectively), bovine fetuin (1 or 0 mg/ml) and O2 (5 or 20 v/v) were examined. Half of the follicles in each culture condition received rhLH on Day 3040. Follicles that reached antral stage were treated with rh chorionic gonadotrophin for 34 h to initiate oocyte meiotic maturation. Media were analyzed for ovarian steroids and anti-mllerian hormone (AMH).ResultsImproved culture conditions supported non-human primate, secondary follicle growth to the antral stage and, for the first time, promoted oocyte maturation to the MII stage. In the presence of fetuin at 5 O2, follicles had the highest survival rate if cultured with high or medium FSH, whereas follicles grew to larger diameters at Week 5 in low FSH. Oocyte health and maturation were promoted under 5 O2. High FSHstimulated steroid production by growing follicles, and steroidogenesis by follicles cultured with low FSH was promoted by LH. AMH biosynthesis was elevated with high compared with low FSH and for longer under 5 O2 than under 20 O2. Conclusions This encapsulated 3D culture model permits further studies on the endocrine and local factors that influence primate follicle growth and oocyte maturation, with relevance to enhancing fertility preservation options in women.

    Original languageEnglish (US)
    Pages (from-to)1061-1072
    Number of pages12
    JournalHuman Reproduction
    Volume26
    Issue number5
    DOIs
    StatePublished - May 2011

    Fingerprint

    Fetuins
    Macaca mulatta
    Gonadotropins
    Primates
    Oocytes
    Oxygen
    Steroids
    Growth
    Hormones
    Human Follicle Stimulating Hormone
    Fertility Preservation
    In Vitro Oocyte Maturation Techniques
    Follicular Phase
    Chorionic Gonadotropin
    Ovary
    Survival Rate
    Antral
    Health
    alginic acid

    Keywords

    • fetuin
    • follicle culture
    • follicle-stimulating hormone
    • luteinizing hormone
    • oxygen

    ASJC Scopus subject areas

    • Rehabilitation
    • Obstetrics and Gynecology
    • Reproductive Medicine

    Cite this

    Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys : Effects of gonadotrophins, oxygen and fetuin. / Xu, Jing; Lawson, M. S.; Yeoman, R. R.; Pau, K. Y.; Barrett, S. L.; Zelinski, Mary; Stouffer, Richard.

    In: Human Reproduction, Vol. 26, No. 5, 05.2011, p. 1061-1072.

    Research output: Contribution to journalArticle

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    abstract = "Background: An alginate-based matrix supports the three-dimensional (3D) architecture of non-human primate follicles and, in the presence of FSH, permits the in vitro development of pre-antral follicles to the small antral stage, including the production of ovarian steroids and paracrine factors. The current study investigated the ability of gonadotrophins, fetuin and oxygen (O 2) to improve primate follicle growth and oocyte maturation in vitro.MethodsMacaque secondary follicles were isolated from the early follicular phase ovaries, encapsulated in a sodium alginate matrix and cultured individually for 40 days in supplemented medium. The effects of recombinant human (rh) FSH (15, 3 and 0.3 ng/ml for high, medium and low FSH, respectively), bovine fetuin (1 or 0 mg/ml) and O2 (5 or 20 v/v) were examined. Half of the follicles in each culture condition received rhLH on Day 3040. Follicles that reached antral stage were treated with rh chorionic gonadotrophin for 34 h to initiate oocyte meiotic maturation. Media were analyzed for ovarian steroids and anti-mllerian hormone (AMH).ResultsImproved culture conditions supported non-human primate, secondary follicle growth to the antral stage and, for the first time, promoted oocyte maturation to the MII stage. In the presence of fetuin at 5 O2, follicles had the highest survival rate if cultured with high or medium FSH, whereas follicles grew to larger diameters at Week 5 in low FSH. Oocyte health and maturation were promoted under 5 O2. High FSHstimulated steroid production by growing follicles, and steroidogenesis by follicles cultured with low FSH was promoted by LH. AMH biosynthesis was elevated with high compared with low FSH and for longer under 5 O2 than under 20 O2. Conclusions This encapsulated 3D culture model permits further studies on the endocrine and local factors that influence primate follicle growth and oocyte maturation, with relevance to enhancing fertility preservation options in women.",
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    T1 - Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys

    T2 - Effects of gonadotrophins, oxygen and fetuin

    AU - Xu, Jing

    AU - Lawson, M. S.

    AU - Yeoman, R. R.

    AU - Pau, K. Y.

    AU - Barrett, S. L.

    AU - Zelinski, Mary

    AU - Stouffer, Richard

    PY - 2011/5

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    N2 - Background: An alginate-based matrix supports the three-dimensional (3D) architecture of non-human primate follicles and, in the presence of FSH, permits the in vitro development of pre-antral follicles to the small antral stage, including the production of ovarian steroids and paracrine factors. The current study investigated the ability of gonadotrophins, fetuin and oxygen (O 2) to improve primate follicle growth and oocyte maturation in vitro.MethodsMacaque secondary follicles were isolated from the early follicular phase ovaries, encapsulated in a sodium alginate matrix and cultured individually for 40 days in supplemented medium. The effects of recombinant human (rh) FSH (15, 3 and 0.3 ng/ml for high, medium and low FSH, respectively), bovine fetuin (1 or 0 mg/ml) and O2 (5 or 20 v/v) were examined. Half of the follicles in each culture condition received rhLH on Day 3040. Follicles that reached antral stage were treated with rh chorionic gonadotrophin for 34 h to initiate oocyte meiotic maturation. Media were analyzed for ovarian steroids and anti-mllerian hormone (AMH).ResultsImproved culture conditions supported non-human primate, secondary follicle growth to the antral stage and, for the first time, promoted oocyte maturation to the MII stage. In the presence of fetuin at 5 O2, follicles had the highest survival rate if cultured with high or medium FSH, whereas follicles grew to larger diameters at Week 5 in low FSH. Oocyte health and maturation were promoted under 5 O2. High FSHstimulated steroid production by growing follicles, and steroidogenesis by follicles cultured with low FSH was promoted by LH. AMH biosynthesis was elevated with high compared with low FSH and for longer under 5 O2 than under 20 O2. Conclusions This encapsulated 3D culture model permits further studies on the endocrine and local factors that influence primate follicle growth and oocyte maturation, with relevance to enhancing fertility preservation options in women.

    AB - Background: An alginate-based matrix supports the three-dimensional (3D) architecture of non-human primate follicles and, in the presence of FSH, permits the in vitro development of pre-antral follicles to the small antral stage, including the production of ovarian steroids and paracrine factors. The current study investigated the ability of gonadotrophins, fetuin and oxygen (O 2) to improve primate follicle growth and oocyte maturation in vitro.MethodsMacaque secondary follicles were isolated from the early follicular phase ovaries, encapsulated in a sodium alginate matrix and cultured individually for 40 days in supplemented medium. The effects of recombinant human (rh) FSH (15, 3 and 0.3 ng/ml for high, medium and low FSH, respectively), bovine fetuin (1 or 0 mg/ml) and O2 (5 or 20 v/v) were examined. Half of the follicles in each culture condition received rhLH on Day 3040. Follicles that reached antral stage were treated with rh chorionic gonadotrophin for 34 h to initiate oocyte meiotic maturation. Media were analyzed for ovarian steroids and anti-mllerian hormone (AMH).ResultsImproved culture conditions supported non-human primate, secondary follicle growth to the antral stage and, for the first time, promoted oocyte maturation to the MII stage. In the presence of fetuin at 5 O2, follicles had the highest survival rate if cultured with high or medium FSH, whereas follicles grew to larger diameters at Week 5 in low FSH. Oocyte health and maturation were promoted under 5 O2. High FSHstimulated steroid production by growing follicles, and steroidogenesis by follicles cultured with low FSH was promoted by LH. AMH biosynthesis was elevated with high compared with low FSH and for longer under 5 O2 than under 20 O2. Conclusions This encapsulated 3D culture model permits further studies on the endocrine and local factors that influence primate follicle growth and oocyte maturation, with relevance to enhancing fertility preservation options in women.

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    KW - follicle-stimulating hormone

    KW - luteinizing hormone

    KW - oxygen

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