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Quadrupling Efficiency in Production of Genetically Modified Pigs Through Quadrupling efficiency in production of genetically PNAS PLUS modified pigs through improved oocyte maturation Ye Yuana,b,1,2,3, Lee D. Spatea,1, Bethany K. Redela, Yuchen Tiana,b, Jie Zhouc, Randall S. Prathera, and R. Michael Robertsa,b,2 aDivision of Animal Sciences, University of Missouri, Columbia, MO 65211; bBond Life Sciences Center, University of Missouri, Columbia, MO 65211; and cDepartment of Obstetrics, Gynecology and Women’s Health, University of Missouri School of Medicine, Columbia, MO 65212 Contributed by R. Michael Roberts, May 23, 2017 (sent for review March 15, 2017; reviewed by Marco Conti and Pablo Juan Ross) Assisted reproductive technologies in all mammals are critically Once cumulus–oocyte complexes (COCs) are removed from the dependent on the quality of the oocytes used to produce embryos. follicular environment and placed into culture, a proportion of the For reasons not fully clear, oocytes matured in vitro tend to be much oocytes usually resume meiosis spontaneously. This promiscuous less competent to become fertilized, advance to the blastocyst stage, progression to metaphase II most probably occurs as the result of a and give rise to live young than their in vivo-produced counterparts, reduced influx of cGMP from the surrounding cumulus cells into particularly if they are derived from immature females. Here we show the oocyte. cGMP maintains high intracellular cAMP concentra- that a chemically defined maturation medium supplemented with tions by inhibiting the phosphodiesterase responsible for cAMP three cytokines (FGF2, LIF, and IGF1) in combination, so-called “FLI hydrolysis (15–17). An inappropriate drop in the concentrations of medium,” improves nuclear maturation of oocytes in cumulus–oocyte the cyclic nucleotides that control meiotic resumption causes un- complexes derived from immature pig ovaries and provides a twofold synchronized nuclear and cytoplasmic maturation of the oocytes, increase in the efficiency of blastocyst production after in vitro fertil- thereby compromising their proper development (18). ization. Transfer of such blastocysts to recipient females doubles mean The gonadotrophin-triggered activation of signaling networks litter size to about nine piglets per litter. Maturation of oocytes in FLI during oocyte maturation is normally orchestrated by EGF and medium, therefore, effectively provides a fourfold increase in piglets related factors, and the downstream MAPK1 and MAPK3 (19–21). born per oocyte collected. As they progress in culture, the FLI-matured The activation of MAPK1/3 in granulosa and cumulus cells plays SCIENCES cumulus–oocyte complexes display distinctly different kinetics of a central role in triggering the essential steps of oocyte matura- AGRICULTURAL MAPK activation in the cumulus cells, much increased cumulus cell tion and COC expansion (22, 23). Cumulus cells in antral folli- expansion, and an accelerated severance of cytoplasmic projections cles lack expression of luteinizing hormone (LH) receptors (24). between the cumulus cells outside the zona pellucida and the oocyte Therefore, oocytes collected for IVM often respond poorly to LH within. These events likely underpin the improvement in oocyte qual- (25), and that may result in dysregulated MAPK activation and ityachievedbyusingtheFLImedium. compromised oocyte competence. As a result, medium used for IVM is usually supplemented with FSH and EGF to stimulate LH cumulus cell | embryo development | genetic modification | sensitivity and downstream signaling pathways (1, 25–28). How- in vitro fertilization | MAPK signaling ever, even with these supplements, oocytes of many species still complete maturation quite poorly, suggesting that the necessary n vitro maturation (IVM) of oocytes is a critical step in assisted Ireproductive technologies carried out in species, such as cattle Significance and swine, for generating oocytes capable of being fertilized in vitro and providing healthy young useful for biomedical and The efficiency of production of genetically altered piglets for – agricultural purposes (1 3). IVM is also important for human in agricultural and biomedical purposes is very low, in large part vitro fertilization (IVF) under conditions where exposure of the because of the poor quality of the in vitro-matured oocytes patient to high levels of superovulating regimens of hormones is used to initiate the process. Here, we describe a chemically contraindicated (4–6). Oocytes retrieved from small to medium- defined culture medium that enhances porcine oocyte matu- sized follicles, if cultured appropriately, can resume meiosis and ration and subsequent embryo development to the blastocyst mature to a state in which they can be fertilized. However, attaining stage, and increases the number of offspring born after em- full developmental competence in immature oocytes retrieved from bryo transfer, thereby effectively quadrupling the efficiency of unstimulated ovaries, particularly ones from prepubertal females, piglet production. This research also provides some insights continues to be a challenge (2). In pigs, production of embryos from into the physiological events that lead to oocyte competence IVM oocytes has assumed increasing importance for biomedical and how the efficacy of oocyte in vitro maturation might be applications, especially for introducing genetic changes into animals improved in other species. that might mimic human disease states (7). In creating such models, somatic cell nuclear transfer (SCNT) has allowed gene Author contributions: Y.Y., L.D.S., R.S.P., and R.M.R. designed research; Y.Y., L.D.S., B.K.R., alterations previously engineered into cultured somatic cells by Y.T., and J.Z. performed research; Y.Y. and L.D.S. analyzed data; and Y.Y., L.D.S., B.K.R., various gene-targeting tools to be relocated to enucleated oocytes R.S.P., and R.M.R. wrote the paper. Reviewers: M.C., University of California, San Francisco; and P.J.R., University of (3), and newer CRISPR-Cas9 technologies can even introduce California, Davis. genetic changes directly into fertilized oocytes (zygotes) (8, 9). The Conflict of interest statement: Y.Y., L.D.S., R.S.P., and R.M.R. have a pending patent reliance on slaughterhouse-derived ovaries from immature gilts as a application “Medium Supplement to Increase the Efficiency of Oocyte maturation and source of oocytes markedly reduces the success of such procedures. Embryo Culture in vitro.” In vivo, the mammalian oocyte grows and matures within a so- Freely available online through the PNAS open access option. matic cell compartment consisting of cumulus cells, and gradually 1Y.Y. and L.D.S. contributed equally to this work. acquires meiotic and developmental competence at the antral 2To whom correspondence may be addressed. Email: [email protected] or robertsrm@ follicle stage (10, 11). Oocytes and cumulus cells must interact missouri.edu. harmoniously in terms of their metabolic activities for competence 3Present address: Colorado Center for Reproductive Medicine, Lone Tree, CO 80124. to be attained (12). Oocyte meiotic arrest is maintained by a high This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. level of cAMP, which is largely produced by the oocytes (13, 14). 1073/pnas.1703998114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1703998114 PNAS Early Edition | 1of9 Downloaded by guest on September 28, 2021 signal transduction pathways have been either understimulated or derived from prepubertal gilts after commercial slaughter were inappropriately stimulated. One explanation is that the follicular examined after each had been added to an otherwise standard, environment contains additional, locally produced factors that are chemically defined medium (41, 42). After 42 h, oocytes were in needed to provide adequate support for the complex process of vitro fertilized and cultured for 6 d (41, 42). Whereas addition of follicular growth and oocyte maturation. Accordingly, follicular FGF2 (40–80 ng/mL) (Fig. 1A), LIF (10–40 ng/mL) (Fig. 1B), fluid is sometimes added to the culture medium to enhance and IGF1 (10–80 ng/mL) (Fig. 1C) each individually improved oocyte IVM, although outcomes have not been universally im- the efficiency of producing metaphase II oocytes, none of the proved (2, 29). It seems counterintuitive to include follicular cytokines improved oocyte developmental competence, as de- fluid to encourage oocyte maturation, as it contains oocyte termined by the ability of the zygotes to form blastocysts after IVF. maturation inhibitors, such as hypoxanthine, which arrest oocyte meiosis (30–32). Nevertheless, the beneficial effects of using Effects of FLI on Improving Oocyte Nuclear Maturation, IVF, and SCNT, follicular fluid during IVM in many studies (33–36) provided Embryo Development to the Blastocyst Stage, and Litter Size After clues that its content of growth factors could be beneficial for Embryo Transfer. FGF2 and LIF at their optimal concentrations oocyte maturation. Here, we provide evidence that three cyto- for nuclear maturation (40 ng/mL and 20 ng/mL, respectively) kines, fibroblast growth factor 2 (FGF2), leukemia inhibitory (Fig. 1 A and B) were added in combination to the IVM me- factor (LIF), and insulin-like growth factor 1 (IGF1), each dium. This mix of two factors improved nuclear maturation known to be present in follicular fluid (37–40), when used in beyond that achieved with the single factors but, more impor- combination can provide much improved oocyte competence, tantly, also
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