Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Glucose consumption and gene expression in granulosa cells collected before and after in vitro oocyte maturation in the southern white rhinoceros (Ceratotherium simum simum)

E. Ruggeri https://orcid.org/0000-0003-3543-1903 A * , C. Young A , N. Ravida A , M. A. Sirard B , R. Krisher C , M. de la Rey D , C. Herbst D and B. Durrant https://orcid.org/0000-0001-6019-9865 A
+ Author Affiliations
- Author Affiliations

A Reproductive Sciences, Beckman Center for Conservation Research, San Diego Zoo Wildlife Alliance, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA.

B Departement des Sciences Animales, Centre de Recherce en Reproduction, Développement et Santé Inter-générationnelle (CRDSI), Université Laval, Pavillion Des Services, Local 2732, Quebec, QC G1V 0A6, Canada.

C Genus PLC, 1525 River Road, De Forest, WI 53532, USA.

D Embryo Plus, 41 Hendrik Vrewoerd Avenue, Brits 0250, South Africa.

* Correspondence to: eruggeri@sdzwa.org

Handling Editor: Ryan Cabot

Reproduction, Fertility and Development 34(13) 875-888 https://doi.org/10.1071/RD22071
Published online: 25 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: With two northern white rhinos (NWR) remaining, the continued existence of this species relies on studying their relative, the southern white rhino (SWR).

Aims: (1) Characterise gene expression in granulosa cells (GC) from SWR cumulus oocyte complexes (COCs) prior to (Pre-) and after (Post-) in vitro maturation (IVM), comparing culture media and oocytes from donors treated with or without gonadotropin stimulation prior to ovum recovery; and (2) evaluate COC glucose consumption in spent media.

Methods: COCs were retrieved from four SWRs. Granulosa cells were collected before and after IVM in SDZ or IZW medium. Total RNA was evaluated by qPCR.

Key results: Oocyte maturation was greater in SDZ than IZW media. Expression of genes associated with follicle development increased in Pre-IVM GC. Six genes were differentially expressed in Post-IVM GC from stimulated compared to unstimulated donors. COCs from stimulated animals consumed more glucose. Fifty seven percent of oocytes in SDZ medium consumed all available glucose.

Conclusions: Gene expression changed upon in vitro maturation and gonadotropin stimulation. Higher glucose availability might be needed during IVM.

Implications: This is the first study examining GC gene expression and COC metabolic requirements in rhinoceros, which are critical aspects to optimise IVM of rhinoceros oocytes.

Keywords: assisted reproductive technologies, endangered species, granulosa cell, in vitro maturation, oocyte, ovum pickup, reproduction, rhinoceros.


References

Bols PEJ, Stout TAE (2018) Transvaginal ultrasound-guided oocyte retrieval (OPU: Ovum Pick-Up) in cows and mares. In ‘Animal biotechnology 1’. (Eds H Niemann, C Wrenzycki) pp. 209–233. (Springer: Cham) 10.1007/978-3-319-92327-7_10

Boni, R (2012). Ovum pick-up in cattle: a 25 yr retrospective analysis. Animal Reproduction 9, 362–369.

Campbell, BK, Onions, V, Kendall, NR, Guo, L, and Scaramuzzi, RJ (2010). The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro. Reproduction 140, 541–550.
The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro.Crossref | GoogleScholarGoogle Scholar |

Dias, FCF, Khan, MIR, Sirard, MA, Adams, GP, and Singh, J (2013). Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reproduction 146, 181–191.
Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle.Crossref | GoogleScholarGoogle Scholar |

Donadeu, FX, Fahiminiya, S, Esteves, CL, Nadaf, J, Miedzinska, K, McNeilly, AS, Waddington, D, and Gerard, N (2014). Transcriptome profiling of granulosa and theca cells during dominant follicle development in the horse. Biology of Reproduction 91, 1–12.
Transcriptome profiling of granulosa and theca cells during dominant follicle development in the horse.Crossref | GoogleScholarGoogle Scholar |

Douville, G, and Sirard, M-A (2014). Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles. Journal of Ovarian Research 7, 50.
Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles.Crossref | GoogleScholarGoogle Scholar |

Duffy, DM, and VandeVoort, CA (2011). Maturation and fertilization of nonhuman primate oocytes are compromised by oral administration of a cyclooxygenase-2 inhibitor. Fertility and Sterility 95, 1256–1260.
Maturation and fertilization of nonhuman primate oocytes are compromised by oral administration of a cyclooxygenase-2 inhibitor.Crossref | GoogleScholarGoogle Scholar |

Galli, C, Duchi, R, Colleoni, S, Lagutina, I, and Lazzari, G (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81, 138–151.
Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice.Crossref | GoogleScholarGoogle Scholar |

Gérard, N, Prades, I, Couty, M, Labberté, M, Daels, P, and Duchamp, G (2000). Concentrations of glucose, pyruvate and lactate in relation to follicular growth, preovulatory maturation and oocyte nuclear maturation stage in the mare. Theriogenology 53, 372.

Gilchrist, RB, Lane, M, and Thompson, JG (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Human Reproduction Update 14, 159–177.
Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.Crossref | GoogleScholarGoogle Scholar |

Girard, A, Dufort, I, Douville, G, and Sirard, M-A (2015). Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle. Reproductive Biology and Endocrinology 13, 17.
Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle.Crossref | GoogleScholarGoogle Scholar |

Harris, SE, Leese, HJ, Gosden, RG, and Picton, HM (2009). Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Molecular Reproduction and Development 76, 231–238.
Pyruvate and oxygen consumption throughout the growth and development of murine oocytes.Crossref | GoogleScholarGoogle Scholar |

Hildebrandt, TB, Hermes, R, Colleoni, S, Diecke, S, Holtze, S, Renfree, MB, Stejskal, J, Hayashi, K, Drukker, M, Loi, P, Göritz, F, Lazzari, G, and Galli, C (2018). Embryos and embryonic stem cells from the white rhinoceros. Nature Communications 9, 2589.
Embryos and embryonic stem cells from the white rhinoceros.Crossref | GoogleScholarGoogle Scholar |

Huang, S, and Czech, MP (2007). The GLUT4 glucose transporter. Cell Metabolism 5, 237–252.
The GLUT4 glucose transporter.Crossref | GoogleScholarGoogle Scholar |

Kahraman, S, Çetinkaya, CP, Çetinkaya, M, Tüfekçi, MA, Ekmekçi, CG, and Montag, M (2018). Is there a correlation between follicle size and gene expression in cumulus cells and is gene expression an indicator of embryo development? Reproductive Biology and Endocrinology 16, 69.
Is there a correlation between follicle size and gene expression in cumulus cells and is gene expression an indicator of embryo development?Crossref | GoogleScholarGoogle Scholar |

Khan, DR, Fournier, É, Dufort, I, Richard, FJ, Singh, J, and Sirard, MA (2016). Meta-analysis of gene expression profiles in granulosa cells during folliculogenesis. Reproduction 151, R103–R110.
Meta-analysis of gene expression profiles in granulosa cells during folliculogenesis.Crossref | GoogleScholarGoogle Scholar |

Kuo, F-T, Fan, K, Ambartsumyan, G, Menon, P, Ketefian, A, Bentsi-Barnes, IK, and Pisarska, MD (2011). Relative expression of genes encoding SMAD signal transduction factors in human granulosa cells is correlated with oocyte quality. Journal of Assisted Reproduction and Genetics 28, 931–938.
Relative expression of genes encoding SMAD signal transduction factors in human granulosa cells is correlated with oocyte quality.Crossref | GoogleScholarGoogle Scholar |

Lewis, N, Hinrichs, K, Leese, HJ, McG, AC, Brison, DR, and Sturmey, R (2020). Energy metabolism of the equine cumulus oocyte complex during in vitro maturation. Scientific Reports 10, 3493.
Energy metabolism of the equine cumulus oocyte complex during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |

Munakata, Y, Kawahara-Miki, R, Shiratsuki, S, Tasaki, H, Itami, N, Shirasuna, K, Kuwayama, T, and Iwata, H (2016). Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in in vitro grown oocyte-and-granulosa cell complexes. Journal of Reproduction and Development 62, 359–366.

Nivet, A-L, Vigneault, C, Blondin, P, and Sirard, M-A (2013). Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–565.
Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine.Crossref | GoogleScholarGoogle Scholar |

Nogueira, MFG, Buratini, J, Price, CA, Castilho, ACS, Pinto, MGL, and Barros, CM (2007). Expression of LH receptor mRNA splice variants in bovine granulosa cells: changes with follicle size and regulation by FSH in vitro. Molecular Reproduction and Development 74, 680–686.
Expression of LH receptor mRNA splice variants in bovine granulosa cells: changes with follicle size and regulation by FSH in vitro.Crossref | GoogleScholarGoogle Scholar |

Reddy, P, Liu, L, Adhikari, D, Jagarlamudi, K, Rajareddy, S, Shen, Y, Du, C, Tang, W, Hämäläinen, T, Peng, SL, Lan, Z-J, Cooney, AJ, Huhtaniemi, I, and Liu, K (2008). Oocyte-specific deletion of pten causes premature activation of the primordial follicle pool. Science 319, 611–613.
Oocyte-specific deletion of pten causes premature activation of the primordial follicle pool.Crossref | GoogleScholarGoogle Scholar |

Roberts, R, Stark, J, Iatropoulou, A, Becker, DL, Franks, S, and Hardy, K (2004). Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biology of Reproduction 71, 199–209.
Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation.Crossref | GoogleScholarGoogle Scholar |

Shin, B, Feser, R, Nault, B, Hunter, S, Maiti, S, Ugwuagbo, KC, and Majumder, M (2019). miR526b and miR655 induce oxidative stress in breast cancer. International Journal of Molecular Sciences 20, 4039.

Sturmey, RG, and Leese, HJ (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.
Energy metabolism in pig oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar |

Sugiura, K, Pendola, FL, and Eppig, JJ (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Developmental Biology 279, 20–30.
Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.Crossref | GoogleScholarGoogle Scholar |

Sutton, ML, Gilchrist, RB, and Thompson, JG (2003a). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Human Reproduction Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity.Crossref | GoogleScholarGoogle Scholar |

Sutton, ML, Cetica, PD, Beconi, MT, Kind, KL, Gilchrist, RB, and Thompson, JG (2003b). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.

Sutton-McDowall, ML, Gilchrist, RB, and Thompson, JG (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |

Thomas, FH, and Vanderhyden, BC (2006). Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reproductive Biology and Endocrinology 4, 19.
Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth.Crossref | GoogleScholarGoogle Scholar |

Uppangala, S, Fernandes, G, Salian, SR, Kumar, P, Talevi, R, Kalthur, G, and Adiga, SK (2020). Reduced ovarian response to controlled ovarian stimulation is associated with increased oxidative stress in the follicular environment. Reproductive Biology 20, 402–407.
Reduced ovarian response to controlled ovarian stimulation is associated with increased oxidative stress in the follicular environment.Crossref | GoogleScholarGoogle Scholar |

Xie, H-L, Wang, Y-B, Jiao, G-Z, Kong, D-L, Li, Q, Li, H, Zheng, L-L, and Tan, J-H (2016). Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Scientific Reports 6, 20764.
Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Yuan, Y, Wheeler, MB, and Krisher, RL (2012). Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence. Biology of Reproduction 87, 78.
Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence.Crossref | GoogleScholarGoogle Scholar |

Zahmel, J, Mundt, H, Jewgenow, K, and Braun, BC (2017). Analysis of gene expression in granulosa cells post-maturation to evaluate oocyte culture systems in the domestic cat. Reproduction in Domestic Animals 52, 65–70.
Analysis of gene expression in granulosa cells post-maturation to evaluate oocyte culture systems in the domestic cat.Crossref | GoogleScholarGoogle Scholar |

Zhang, H, Du, Y, Zhang, X, Lu, J, and Holmgren, A (2014). Glutaredoxin 2 reduces both thioredoxin 2 and thioredoxin 1 and protects cells from apoptosis induced by auranofin and 4-hydroxynonenal. Antioxidants & Redox Signaling 21, 669–681.
Glutaredoxin 2 reduces both thioredoxin 2 and thioredoxin 1 and protects cells from apoptosis induced by auranofin and 4-hydroxynonenal.Crossref | GoogleScholarGoogle Scholar |