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Expression levels of FSHR, IGF1R, CYP11al and HSD3β in cumulus cells can predict in vitro developmental competence of bovine oocytes

Published online by Cambridge University Press:  02 June 2020

Atchalalt Khurchabilig Open the ORCID record for Atchalalt Khurchabilig [Opens in a new window] ,
Akane Sato ,
Shiori Ashibe ,
Asuka Hara ,
Rika Fukumori  and
Yoshikazu Nagao
Atchalalt Khurchabilig
Affiliation:
Department of Animal Production Science, United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo183–8509, Japan University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
Akane Sato
Affiliation:
University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
Shiori Ashibe
Affiliation:
Department of Animal Production Science, United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo183–8509, Japan University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
Asuka Hara
Affiliation:
University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
Rika Fukumori
Affiliation:
University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
Yoshikazu Nagao*
Affiliation:
Department of Animal Production Science, United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo183–8509, Japan University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi321–4415, Japan
*
Author for correspondence: Yoshikazu Nagao. University Farm, Faculty of Agriculture, Utsunomiya University, Tochigi, Japan. Tel:/Fax: +81 285 84 2426. E-mail: [email protected]
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Summary

The efficiency of in vitro embryo production technologies would be improved by the development of suitable non-invasive biomarkers that allow the selection of good quality cumulus–oocyte complexes (COCs). The present study used whole, single oocyte culture to investigate whether the expression levels of follicle-stimulating hormone receptor (FSHR), insulin-like factor 1 receptor (IGF1R) and three steroidogenesis-related enzymes (CYP11al, CYP19al and HSD3β) in cumulus cells reflected the developmental competence of COCs. Cumulus cells were collected from single COCs before maturation culture and relative mRNA levels were assessed using real-time PCR. The analysis indicated that mRNAs for FSHR, IGF1R, CYP11al and HSD3β were present at higher levels in cumulus cells from COCs that failed to form blastocysts compared with cumulus cells from COCs that formed blastocysts. Moreover, FSHR and IGF1R mRNA levels were positively correlated with those of genes for steroidogenesis-related enzymes. In conclusion, poor developmental competence of COCs was related to higher expression of FSHR, IGF1R, CYP11al and HSD3β in cumulus cells, which may indicate the advanced differentiation of cumulus cells into granulosa cells.

Keywords

BiomarkersBovine oocyteCumulus cellDevelopmental competencemRNA
Type
Research Article
Information
Zygote , Volume 28 , Issue 5 , October 2020 , pp. 425 - 431
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

Present address: Department of Health and Environmental Science, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido 069-8501, Japan.

References

Ai-Katanani, YM, Et, Al, Paula-Lopes, FF and Hansen, PJ (2002). Effect of season and exposure to heat stress on oocyte competence in Holstein cows. J Dairy Sci 85, 390–96.CrossRefGoogle Scholar
Aparicio, IM, Garcia-Herreros, M, O’Shea, LC, Hensey, C, Lonergan, P and Fair, T (2011). Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod 84, 910–21.CrossRefGoogle ScholarPubMed
Baumgarten, SC, Convissar, SM, Fierro, MA, Winston, NJ, Scoccia, B and Stocco, C (2014). IGF1R signaling is necessary for FSH-induced activation of AKT and differentiation of human cumulus granulosa cells. J Clin Endocrinol Metab 99, 2995–3004.CrossRefGoogle ScholarPubMed
Bettegowda, A, Patel, OV, Lee, KB, Park, KE, Salem, M, Yao, J, Ireland, JJ and Smith, GW (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol Reprod 79, 301–9.CrossRefGoogle ScholarPubMed
Borjigin, S, Ogata, K, Taguchi, Y, Kato, Y and Nagao, Y (2013). The developmental potential of oocytes is impaired in cattle with liver abnormalities. J Reprod Dev 59, 163–73.Google Scholar
Carolan, C, Lonergan, P, Khatir, H and Mermillod, P (1996). In vitro production of bovine embryos using individual oocytes. Mol Reprod Dev 45, 145–50.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Corcoran, D, Fair, T, Park, S, Rizos, D, Patel, OV, Smith, GW, Coussens, PM, Ireland, JJ, Boland, MP, Evans, AC and Lonergan, P (2006). Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Reproduction 131, 651–60.CrossRefGoogle ScholarPubMed
Diaz, FJ, Wigglesworth, K and Eppig, JJ (2007). Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120, 1330–40.CrossRefGoogle ScholarPubMed
First, NL, Leibfried-Rutledge, ML and Sirard, MA (1988). Cytoplasmic control of oocyte maturation and species differences in the development of maturational competence. Prog Clin Biol Res 267, 1–46.Google ScholarPubMed
Gasperin, BG, Ferreira, R, Rovani, MT, Santos, JT, Buratini, J, Price, CA and Goncalves, PB (2012). FGF10 inhibits dominant follicle growth and estradiol secretion in vivo in cattle. Reproduction 143, 815–23.CrossRefGoogle ScholarPubMed
Hosoe, M, Kaneyama, K, Ushizawa, K, Hayashi, K and Takahashi, T (2011). Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod Biol Endocrinol 9, 33–40.CrossRefGoogle ScholarPubMed
Hussein, TS, Thompson, JG and Gilchrist, RB (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 296, 514–21.CrossRefGoogle ScholarPubMed
Kussano, NR, Leme, LO, Guimaraes, AL, Franco, MM and Dode, MA (2016). Molecular markers for oocyte competence in bovine cumulus cells. Theriogenology 85, 1167–76.CrossRefGoogle ScholarPubMed
Leroy, JL, Van Soom, A, Opsomer, G, Goovaerts, IG and Bols, PE (2008). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high-yielding dairy cows. Reprod Domest Anim 43, 623–32.CrossRefGoogle ScholarPubMed
Li, R, Norman, RJ, Armstrong, DT and Gilchrist, RB (2000). Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod 63, 839–45.CrossRefGoogle ScholarPubMed
Lonergan, P, Monaghan, P, Rizos, D, Boland, MP and Gordon, I (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol Reprod Dev 37, 48–53.CrossRefGoogle ScholarPubMed
Lonergan, P, Rizos, D, Gutierrez-Adan, Fair T and Boland, M (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod Domest Anim 38, 259–67.CrossRefGoogle ScholarPubMed
Melo, EO, Cordeiro, DM, Pellegrino, R, Wei, Z, Daye, ZJ, Nishimura, RC and Dode, MA (2017). Identification of molecular markers for oocyte competence in bovine cumulus cells. Anim Genet 48, 19–29.CrossRefGoogle ScholarPubMed
Memili, E and First, NL (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.CrossRefGoogle ScholarPubMed
Nagao, Y, Iijima, R and Saeki, K (2008). Interaction between embryos and culture conditions during in vitro development of bovine early embryos. Zygote 16, 127–33.CrossRefGoogle ScholarPubMed
Nagao, Y, Ohta, Y, Murakami, H and Kato, Y (2010). The effects of methyl-beta-cyclodextrin on in vitro fertilization and the subsequent development of bovine oocytes. Zygote 18, 323–30.CrossRefGoogle ScholarPubMed
Nagao, Y, Saeki, K, Hoshi, M, Takahashi, Y, Kanagawa, H (1995). Effects of water quality on in vitro fertilization and development of bovine oocytes in protein-free medium. Theriogenology 44, 433–44.CrossRefGoogle ScholarPubMed
Nivet, AL, Bunel, A, Labrecque, R, Belanger, J, Vigneault, C, Blondin, P and Sirard, MA (2012). FSH withdrawal improves developmental competence of oocytes in the bovine model. Reproduction 143, 165–71.CrossRefGoogle ScholarPubMed
Nivet, AL, Vigneault, C, Blondin, P and Sirard, MA (2013). Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–65.CrossRefGoogle ScholarPubMed
Oktem, O, Akin, N, Bildik, G, Yakin, K, Alper, E, Balaban, B and Urman, B (2017). FSH stimulation promotes progesterone synthesis and output from human granulosa cells without luteinization. Hum Reprod 32, 643–52.CrossRefGoogle ScholarPubMed
Otsuka, F, Yamamoto, S, Erickson, GF and Shimasaki, S (2001). Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J Biol Chem 276, 11387–92.CrossRefGoogle ScholarPubMed
Otsuka, F, Yao, Z, Lee, T, Yamamoto, S, Erickson, GF and Shimasaki, S (2000). Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 275, 39523–28.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, MP and Lonergan, P (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 61, 234–48.CrossRefGoogle ScholarPubMed
Roth, Z, Dvir, A, Kalo, D, Lavon, Y, Krifucks, O, Wolfenson, D and Leitner, G (2013). Naturally occurring mastitis disrupts developmental competence of bovine oocytes. J Dairy Sci 96, 6499–505.CrossRefGoogle ScholarPubMed
Silva, CC and Knight, PG (2000). Effects of androgens, progesterone and their antagonists on the developmental competence of in vitro matured bovine oocytes. J Reprod Fertil 119, 261–9.CrossRefGoogle ScholarPubMed
Sugimura, S, Akai, T, Hashiyada, Y, Aikawa, Y, Ohtake, M, Matsuda, H, Kobayashi, S, Kobayashi, E, Konishi, K and Imai, K (2013). Effect of embryo density on in vitro development and gene expression in bovine in vitro-fertilized embryos cultured in a microwell system. J Reprod Dev 59, 115–22.CrossRefGoogle Scholar
Su, YQ, Sugiura, K and Eppig, JJ (2009). Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27, 32–42.CrossRefGoogle ScholarPubMed
Tanghe, S, Van Soom, A, Nauwynck, H, Coryn, M and De Kruif, A (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61, 414–24.CrossRefGoogle ScholarPubMed
Torner, H, Ghanem, N, Ambros, C, Holker, M, Tomek, W, Phatsara, C, Alm, H, Sirard, MA, Kanitz, W, Schellander, K and Tesfaye, D (2008). Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197–212.CrossRefGoogle ScholarPubMed
Vassena, R, Mapletoft, RJ, Allodi, S, Singh, J and Adams, GP (2003). Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology 60, 923–32.CrossRefGoogle ScholarPubMed
Ward, F, Enright, B, Rizos, D, Boland, M and Lonergan, P (2002). Optimization of in vitro bovine embryo production: effect of duration of maturation, length of gamete co-incubation, sperm concentration and sire. Theriogenology 57, 2105–17.CrossRefGoogle ScholarPubMed
Weller, MMDCA, Fortes, MRS, Marcondes, MI, Rotta, PP, Gionbeli, TRS, Valadares Filho, SC, Campos, MM, Silva, FF, Silva, W, Moore, S and Guimaraes, SEF (2016). Effect of maternal nutrition and days of gestation on pituitary gland and gonadal gene expression in cattle. J Dairy Sci 99, 3056–71.CrossRefGoogle ScholarPubMed
Zhang, M, Su, YQ, Sugiura, K, Xia, G and Eppig, JJ (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–9.CrossRefGoogle ScholarPubMed
Zhou, P, Baumgarten, SC, Wu, Y, Bennett, J, Winston, N, Hirshfeld-Cytron, J and Stocco, C (2013). IGF-I signaling is essential for FSH stimulation of AKT and steroidogenic genes in granulosa cells. Mol Endocrinol 27, 511–23.CrossRefGoogle ScholarPubMed