Parameters influencing the maturation of bovine oocyte: a review
Sandra Duarte-da-Fonseca Dias
A B , Ana Palmeira-de-Oliveira A C D , Joana Rolo A , Patrícia Gomes-Ruivo A C E , António Hélio Oliani C E F , Rita Palmeira-de-Oliveira A C D G , José Martinez-de-Oliveira A and Luís Pinto-de-Andrade B H *
+ Author Affiliations
- Author Affiliations
A CICS-UBI – Health Sciences Research Centre, University of Beira Interior, Covilhã, Portugal.
B Escola Superior Agrária do Instituto Politécnico de Castelo Branco, Castelo Branco, Portugal.
C FCS-UBI – School of Health Sciences, University of Beira Interior, Covilhã, Portugal.
D Labfit-HPRD: Health Products Research and Development Lda, Covilhã, Portugal.
E CHUCB: Centro Hospitalar Universitário Cova da Beira, EPE, Reproductive Medicine Unit, Covilhã, Portugal.
F São José do Rio Preto School of Medicine FAMERP, São José do Rio Preto, São Paulo, Brazil.
G Faculty of Medicine (Polo 1), CNC – Center for Neurosciences and Cell Biology, Center for Innovative Biomedicine and Biotechnology (CIBB), University of Coimbra, Coimbra, Portugal.
H CERNAS: Research Center for Natural Resources, Environment and Society, Agriculture Science Research Group, Castelo Branco, Portugal.
Animal Production Science - https://doi.org/10.1071/AN21380
Submitted: 23 July 2021 Accepted: 5 April 2022 Published online: 3 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
During the past decades, pharmaceutical companies have been making efforts to find alternative methods to animal-based tests. Several tests have been proposed as models for in vitro testing, including oocyte and bovine embryo produced in vitro in developmental toxicity screening. Under optimal experimental conditions, the in vitro maturation rate of bovine oocytes approaches 90%, the fertilisation rate is close to 80%; however, the success in progressing to blastocyst is almost half of those, attaining only 30–40%. It is also known that after in vivo insemination of normally cycling cows, approximately 85% of the ovulated oocytes will develop into an embryo. In contrast to this, in most in vitro production practises, only 15–20% of the oocytes punctured yield transferable embryos. In fact, from oocyte to embryo development, the competency of the female gamete is mandatory to assure the repeatability and feasibility of the results. The developmental competency of an oocyte can be influenced by several factors, including external components: such as the age of the cow, its nutritional status, body condition score, genetic merit for milk yield, proper function of intracellular molecular mechanisms, as well as the season. In this review, the factors influencing the quality of bovine oocytes that could possibly influence the success of producing embryos in vitro are highlighted.
Keywords: bovine, cryopreservation, folliculogenesis, in vitro fertilisation, nutrition, oocyte competence, oocyte maturation, reproductive status.
References
Abdelatty AM, Iwaniuk ME, Potts SB, Gad A (2018) Influence of maternal nutrition and heat stress on bovine oocyte and embryo development. International Journal of Veterinary Science and Medicine 6, S1–S5.| Influence of maternal nutrition and heat stress on bovine oocyte and embryo development.Crossref | GoogleScholarGoogle Scholar | 30761314PubMed |
Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology 3, 28
| Role of oxidative stress in female reproduction.Crossref | GoogleScholarGoogle Scholar | 16018814PubMed |
Aguila L, Treulen F, Therrien J, Felmer R, Valdivia M, Smith LC (2020) Oocyte selection for in vitro embryo production in bovine species: noninvasive approaches for new challenges of oocyte competence. Animals 10, 2196
| Oocyte selection for in vitro embryo production in bovine species: noninvasive approaches for new challenges of oocyte competence.Crossref | GoogleScholarGoogle Scholar |
Ali A, Coenen K, Bousquet D, Sirard M-A (2004) Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes. Theriogenology 62, 1596–1606.
| Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15511547PubMed |
Arav A (2014) Cryopreservation of oocytes and embryos. Theriogenology 81, 96–102.
| Cryopreservation of oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 24274414PubMed |
Bahrami M, Morris MB, Day ML (2019) Amino acid supplementation of a simple inorganic salt solution supports efficient in vitro maturation (IVM) of bovine oocytes. Scientific Reports 9, 11739
| Amino acid supplementation of a simple inorganic salt solution supports efficient in vitro maturation (IVM) of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 31409817PubMed |
Beker van Woudenberg A, Gröllers-Mulderij M, Snel C, Jeurissen N, Stierum R, Wolterbeek A (2012) The bovine oocyte in vitro maturation model: a potential tool for reproductive toxicology screening. Reproductive Toxicology 34, 251–260.
| The bovine oocyte in vitro maturation model: a potential tool for reproductive toxicology screening.Crossref | GoogleScholarGoogle Scholar | 22664270PubMed |
Bellin ME, Ax RL (1987) Purification of glycosaminoglycans from bovine follicular fluid. Journal of Dairy Science 70, 1913–1919.
| Purification of glycosaminoglycans from bovine follicular fluid.Crossref | GoogleScholarGoogle Scholar | 2959689PubMed |
Bevers MM, Dieleman SJ, van den Hurk R, Izadyar F (1997) Regulation and modulation of oocyte maturation in the bovine. Theriogenology 47, 13–22.
| Regulation and modulation of oocyte maturation in the bovine.Crossref | GoogleScholarGoogle Scholar |
Boland MP, Lonergan P, O’Callaghan D (2001) Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55, 1323–1340.
| Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development.Crossref | GoogleScholarGoogle Scholar | 11327687PubMed |
Boni R (2012) Origins and effects of oocyte quality in cattle. Animal Reproduction 9, 333–340. https://www.animal-reproduction.org/article/5b5a6059f7783717068b46ef/pdf/animreprod-9-3-333.pdf
Botigelli RC, Razza EM, Pioltine EM, Gouveia Nogueira MF (2017) New approaches regarding the in vitro maturation of oocytes: manipulating cyclic nucleotides and their partners in crime. Jornal Brasileiro de Reproducao Assistida 21, 35–44.
| New approaches regarding the in vitro maturation of oocytes: manipulating cyclic nucleotides and their partners in crime.Crossref | GoogleScholarGoogle Scholar |
Bourdon G, Cadoret V, Charpigny G, Couturier-Tarrade A, Dalbies-Tran R, Flores MJ, Froment P, Raliou M, Reynaud K, Saint-Dizier M, Jouneau A (2021) Progress and challenges in developing organoids in farm animal species for the study of reproduction and their applications to reproductive biotechnologies. Veterinary Research 52, 42
| Progress and challenges in developing organoids in farm animal species for the study of reproduction and their applications to reproductive biotechnologies.Crossref | GoogleScholarGoogle Scholar | 33691745PubMed |
Brambillasca F, Guglielmo MC, Coticchio G, Mignini Renzini M, Dal Canto M, Fadini R (2013) The current challenges to efficient immature oocyte cryopreservation. Journal of Assisted Reproduction and Genetics 30, 1531–1539.
| The current challenges to efficient immature oocyte cryopreservation.Crossref | GoogleScholarGoogle Scholar | 24114631PubMed |
Brodin T, Hadziosmanovic N, Berglund L, Olovsson M, Holte J (2013) Antimüllerian hormone levels are strongly associated with live-birth rates after assisted reproduction. Journal of Clinical Endocrinology & Metabolism 98, 1107–1114.
| Antimüllerian hormone levels are strongly associated with live-birth rates after assisted reproduction.Crossref | GoogleScholarGoogle Scholar |
Budna J, Rybska M, Ciesiółka S, Bryja A, Borys S, Kranc W, Wojtanowicz-Markiewicz K, Jeseta M, Sumelka E, Bukowska D, Antosik P, Brüssow KP, Bruska M, Nowicki M, Zabel M, Kempisty B (2017) Expression of genes associated with BMP signaling pathway in porcine oocytes before and after IVM – a microarray approach. Reproductive Biology and Endocrinology 15, 43
| Expression of genes associated with BMP signaling pathway in porcine oocytes before and after IVM – a microarray approach.Crossref | GoogleScholarGoogle Scholar | 28576120PubMed |
Castro SV, Carvalho AA, Silva CMG, Santos FW, Campello CC, Figueiredo JR, Rodrigues APR (2014) Fresh and vitrified bovine preantral follicles have different nutritional requirements during in vitro culture. Cell and Tissue Banking 15, 591–601.
| Fresh and vitrified bovine preantral follicles have different nutritional requirements during in vitro culture.Crossref | GoogleScholarGoogle Scholar | 24610241PubMed |
Chian R-C, Chung J-T, Downey BR, Lin Tan S (2002) Maturational and developmental competence of immature oocytes retrieved from bovine ovaries at different phases of folliculogenesis. Reproductive BioMedicine Online 4, 127–132.
| Maturational and developmental competence of immature oocytes retrieved from bovine ovaries at different phases of folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 12470574PubMed |
Chowdhury MMR, Choi BH, Khan I, Lee KL, Mesalam A, Song SH, Xu L, Joo MD, Afrin F, Kong IK (2017) Supplementation of lycopene in maturation media improves bovine embryo quality in vitro. Theriogenology 103, 173–184.
| Supplementation of lycopene in maturation media improves bovine embryo quality in vitro.Crossref | GoogleScholarGoogle Scholar | 28800556PubMed |
Denker BM, Nigam SK (1998) Molecular structure and assembly of the tight junction. American Journal of Physiology - Renal Physiology 274, F1–F9.
| Molecular structure and assembly of the tight junction.Crossref | GoogleScholarGoogle Scholar |
Diskin MG, Mackey DR, Roche JF, Sreenan JM (2003) Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Animal Reproduction Science 78, 345–370.
| Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle.Crossref | GoogleScholarGoogle Scholar | 12818653PubMed |
Domínguez MM (1995) Effects of body condition, reproductive status and breed on follicular population and oocyte quality in cows. Theriogenology 43, 1405–1418.
| Effects of body condition, reproductive status and breed on follicular population and oocyte quality in cows.Crossref | GoogleScholarGoogle Scholar |
Erickson GF, Danforth DR (1995) Ovarian control of follicle development. American Journal of Obstetrics and Gynecology 172, 736–747.
| Ovarian control of follicle development.Crossref | GoogleScholarGoogle Scholar | 7872375PubMed |
European Centre for the validation of Alternative Methods (ECVAM) (1996) DB-ALM protocol no 129: Toxicity test on in vitro maturation of bovine oocytes, 1–7. Available at http://cidportal.jrc.ec.europa.eu/ftp/jrc-opendata/EURL-ECVAM/datasets/DBALM/LATEST/online/DBALM_docs/129_M_Oocyte%20In%20Vitro%20Maturation%20Assay.pdf
European Centre for the validation of Alternative Methods (ECVAM) (2011) EU integrated Project – ReProTect – Development of a novel approach in hazard and risk assessment for reproductive toxicity by a combination and application of in vitro, tissue and sensor technologies (2004–2009), 1–4. Available at http://cidportal.jrc.ec.europa.eu/ftp/jrc-opendata/EURL-ECVAM/datasets/DBALM/LATEST/online/DBALM_docs/PR_reprotect.pdf
Faber DC, Molina JA, Ohlrichs CL, Vander Zwaag DF, Ferré LB (2003) Commercialization of animal biotechnology. Theriogenology 59, 125–138.
| Commercialization of animal biotechnology.Crossref | GoogleScholarGoogle Scholar | 12499024PubMed |
Fair T (2013) Molecular and endocrine determinants of oocyte competence. Animal Reproduction 10, 277–282.
Fatehi AN, van Den Hurk R, Colenbrander B, Daemen AJJM, van Tol HTA, Monteiro RM, Roelen BAJ, Bevers MM (2005) Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–889.
| Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development.Crossref | GoogleScholarGoogle Scholar | 15629804PubMed |
Feugang JM, Camargo-Rodríguez O, Memili E (2009) Culture systems for bovine embryos. Livestock Science 121, 141–149.
| Culture systems for bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Fleming R, Seifer DB, Frattarelli JL, Ruman J (2015) Assessing ovarian response: antral follicle count versus anti-Müllerian hormone. Reproductive BioMedicine Online 31, 486–496.
| Assessing ovarian response: antral follicle count versus anti-Müllerian hormone.Crossref | GoogleScholarGoogle Scholar | 26283017PubMed |
Fouladi-Nashta AA, Gutierrez CG, Gong JG, Garnsworthy PC, Webb R (2007) Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biology of Reproduction 77, 9–17.
| Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 17344470PubMed |
Fry RC, Niall EM, Simpson TL, Squires TJ, Reynolds J (1997) The collection of oocytes from bovine ovaries. Theriogenology 47, 977–987.
| The collection of oocytes from bovine ovaries.Crossref | GoogleScholarGoogle Scholar | 16728047PubMed |
Furnus CC, de Matos DG, Picco S, García PP, Inda AM, Mattioli G, Errecalde AL (2008) Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Animal Reproduction Science 109, 88–99.
| Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes.Crossref | GoogleScholarGoogle Scholar | 18242890PubMed |
Galli C, Duchi R, Crotti G, Turini P, Ponderato N, Colleoni S, Lagutina I, Lazzari G (2003) Bovine embryo technologies. Theriogenology 59, 599–616.
| Bovine embryo technologies.Crossref | GoogleScholarGoogle Scholar | 12499007PubMed |
García-Martínez T, Vendrell-Flotats M, Martínez-Rodero I, Ordóñez-León EA, Álvarez-Rodríguez M, López-Béjar M, Yeste M, Mogas T (2020) Glutathione ethyl ester protects in vitro-maturing bovine oocytes against oxidative stress induced by subsequent vitrification/warming. International Journal of Molecular Sciences 21, 7547
| Glutathione ethyl ester protects in vitro-maturing bovine oocytes against oxidative stress induced by subsequent vitrification/warming.Crossref | GoogleScholarGoogle Scholar |
Gosden RG, Sadler IH, Reed D, Hunter RHF (1990) Characterization of ovarian follicular fluids of sheep, pigs and cows using proton nuclear magnetic resonance spectroscopy. Experientia 46, 1012–1015.
| Characterization of ovarian follicular fluids of sheep, pigs and cows using proton nuclear magnetic resonance spectroscopy.Crossref | GoogleScholarGoogle Scholar | 2171975PubMed |
Gutnisky C, Morado S, Gadze T, Donato A, Alvarez G, Dalvit G, Cetica P (2020) Morphological, biochemical and functional studies to evaluate bovine oocyte vitrification. Theriogenology 143, 18–26.
| Morphological, biochemical and functional studies to evaluate bovine oocyte vitrification.Crossref | GoogleScholarGoogle Scholar | 31830686PubMed |
Hendriksen PJM, Vos PLAM, Steenweg WNM, Bevers MM, Dieleman SJ (2000) Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 53, 11–20.
| Bovine follicular development and its effect on the in vitro competence of oocytes.Crossref | GoogleScholarGoogle Scholar |
Hoelker M, Kassens A, Salilew-Wondim D, Sieme H, Wrenzycki C, Tesfaye D, Neuhoff C, Schellander K, Held-Hoelker E (2017) Birth of healthy calves after intra-follicular transfer (IFOT) of slaughterhouse derived immature bovine oocytes. Theriogenology 97, 41–49.
| Birth of healthy calves after intra-follicular transfer (IFOT) of slaughterhouse derived immature bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28583607PubMed |
Hosseini SM, Nasr-Esfahani MH (2016) What does the cryopreserved oocyte look like? A fresh look at the characteristic oocyte features following cryopreservation. Reproductive BioMedicine Online 32, 377–387.
| What does the cryopreserved oocyte look like? A fresh look at the characteristic oocyte features following cryopreservation.Crossref | GoogleScholarGoogle Scholar | 26907599PubMed |
Huang Z, Wells D (2010) The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Molecular Human Reproduction 16, 715–725.
| The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome.Crossref | GoogleScholarGoogle Scholar | 20435609PubMed |
Hyttel P, Fair T, Callesen H, Greve T (1997) Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
| Oocyte growth, capacitation and final maturation in cattle.Crossref | GoogleScholarGoogle Scholar |
Ipsa E, Cruzat VF, Kagize JN, Yovich JL, Keane KN (2019) Growth hormone and insulin-like growth factor action in reproductive tissues. Frontiers in Endocrinology 10, 777
| Growth hormone and insulin-like growth factor action in reproductive tissues.Crossref | GoogleScholarGoogle Scholar | 31781044PubMed |
Johnson MH (2005) The problematic in-vitro embryo in the age of epigenetics. Reproductive BioMedicine Online 10, 88–96.
| The problematic in-vitro embryo in the age of epigenetics.Crossref | GoogleScholarGoogle Scholar | 15820016PubMed |
Jones A, Bernabé BP, Padmanabhan V, Li J, Shikanov A (2021) Capitalizing on transcriptome profiling to optimize and identify targets for promoting early murine folliculogenesis in vitro. Scientific Reports 11, 12517
| Capitalizing on transcriptome profiling to optimize and identify targets for promoting early murine folliculogenesis in vitro.Crossref | GoogleScholarGoogle Scholar | 34131220PubMed |
Khurana NK, Niemann H (2000) Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 54, 741–756.
| Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 11101035PubMed |
Kim KS, Mitsumizo N, Fujita K, Utsumi K (1996) The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos. Theriogenology 45, 787–799.
| The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Kim JH, Lee JR, Chang HJ, Jee BC, Suh CS, Kim SH (2014) Anti-Müllerian hormone levels in the follicular fluid of the preovulatory follicle: a predictor for oocyte fertilization and quality of embryo. Journal of Korean Medical Science 29, 1266–1270.
| Anti-Müllerian hormone levels in the follicular fluid of the preovulatory follicle: a predictor for oocyte fertilization and quality of embryo.Crossref | GoogleScholarGoogle Scholar | 25246746PubMed |
Le Gal F, Massip A (1999) Cryopreservation of cattle oocytes: effects of meiotic stage, cycloheximide treatment, and vitrification procedure. Cryobiology 38, 290–300.
| Cryopreservation of cattle oocytes: effects of meiotic stage, cycloheximide treatment, and vitrification procedure.Crossref | GoogleScholarGoogle Scholar | 10413572PubMed |
Leibfried-Rutledge ML (1999) Factors determining competence of in vitro produced cattle embryos. Theriogenology 51, 473–485.
| Factors determining competence of in vitro produced cattle embryos.Crossref | GoogleScholarGoogle Scholar | 10729106PubMed |
Li L, Lu X, Dean J (2013) The maternal to zygotic transition in mammals. Molecular Aspects of Medicine 34, 919–938.
| The maternal to zygotic transition in mammals.Crossref | GoogleScholarGoogle Scholar | 23352575PubMed |
Li J, Chen Q, Wang J, Huang G, Ye H (2020) Does growth hormone supplementation improve oocyte competence and IVF outcomes in patients with poor embryonic development? A randomized controlled trial. BMC Pregnancy and Childbirth 20, 310
| Does growth hormone supplementation improve oocyte competence and IVF outcomes in patients with poor embryonic development? A randomized controlled trial.Crossref | GoogleScholarGoogle Scholar | 32434490PubMed |
Luciano AM, Franciosi F, Modina SC, Lodde V (2011) Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biology of Reproduction 85, 1252–1259.
| Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s).Crossref | GoogleScholarGoogle Scholar | 21816847PubMed |
Makita M, Ueda M, Miyano T (2016) The fertilization ability and developmental competence of bovine oocytes grown in vitro. Journal of Reproduction and Development 62, 379–384.
| The fertilization ability and developmental competence of bovine oocytes grown in vitro.Crossref | GoogleScholarGoogle Scholar |
Maller JL, Krebs EG (1980) Regulation of oocyte maturation. Current Topics in Cellular Regulation 16, 271–311.
| Regulation of oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 6249544PubMed |
Marques CC, Santos-Silva C, Rodrigues C, Matos JE, Moura T, Baptista MC, Horta AEM, Bessa RJB, Alves SP, Soveral G, Pereira RMLN (2018) Bovine oocyte membrane permeability and cryosurvival: effects of different cryoprotectants and calcium in the vitrification media. Cryobiology 81, 4–11.
| Bovine oocyte membrane permeability and cryosurvival: effects of different cryoprotectants and calcium in the vitrification media.Crossref | GoogleScholarGoogle Scholar | 29524383PubMed |
Mermillod P, Dalbiès-Tran R, Uzbekova S, Thélie A, Traverso J-M, Perreau C, Papillier P, Monget P (2008) Factors affecting oocyte quality: who is driving the follicle? Reproduction in Domestic Animals 43, 393–400.
| Factors affecting oocyte quality: who is driving the follicle?Crossref | GoogleScholarGoogle Scholar | 18638152PubMed |
Merton JS, de Roos APW, Mullaart E, de Ruigh L, Kaal L, Vos PLAM, Dieleman SJ (2003) Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology 59, 651–674.
| Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry.Crossref | GoogleScholarGoogle Scholar | 12499010PubMed |
Monget P, Fabre S, Mulsant P, Lecerf F, Elsen J-M, Mazerbourg S, Pisselet C, Monniaux D (2002) Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. In Domestic Animal Endocrinology 23, 139–154.
| Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals.Crossref | GoogleScholarGoogle Scholar |
Moussa M, Shu J, Zhang XH, Zeng F (2015) Maternal control of oocyte quality in cattle ‘a review’. Animal Reproduction Science 155, 11–27.
| Maternal control of oocyte quality in cattle ‘a review’.Crossref | GoogleScholarGoogle Scholar | 25726438PubMed |
Otsuka F, Yamamoto S, Erickson GF, Shimasaki S (2001) Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. Journal of Biological Chemistry 276, 11387–11392.
| Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression.Crossref | GoogleScholarGoogle Scholar |
Paes VM, Vieira LA, Correia HHV, Sa NAR, Moura AAA, Sales AD, Rodrigues APR, Magalhães-Padilha DM, Santos FW, Apgar GA, Campello CC, Camargo LSA, Figueiredo JR (2016) Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex. Theriogenology 86, 994–1003.
| Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 27125691PubMed |
Park Y-S, Kim S-S, Kim J-M, Park H-D, Byun M-D (2005) The effects of duration of in vitro maturation of bovine oocytes on subsequent development, quality and transfer of embryos. Theriogenology 64, 123–134.
| The effects of duration of in vitro maturation of bovine oocytes on subsequent development, quality and transfer of embryos.Crossref | GoogleScholarGoogle Scholar | 15935848PubMed |
Rizos D, Ward F, Duffy P, Boland MP, 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. Molecular Reproduction and Development 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 11803560PubMed |
Robinson JJ, Ashworth CJ, Rooke JA, Mitchell LM, McEvoy TG (2006) Nutrition and fertility in ruminant livestock. Animal Feed Science and Technology 126, 259–276.
| Nutrition and fertility in ruminant livestock.Crossref | GoogleScholarGoogle Scholar |
Rocha A, Randel RD, Broussard JR, Lim JM, Blair RM, Roussel JD, Godke RA, Hansel W (1998) High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology 49, 657–665.
| High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows.Crossref | GoogleScholarGoogle Scholar | 10732044PubMed |
Sakaguchi K, Nagano M (2020) Follicle priming by FSH and pre-maturation culture to improve oocyte quality in vivo and in vitro. Theriogenology 150, 122–129.
| Follicle priming by FSH and pre-maturation culture to improve oocyte quality in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 32005509PubMed |
Sanfins A, Rodrigues P, Albertini DF (2018) GDF-9 and BMP-15 direct the follicle symphony. Journal of Assisted Reproduction and Genetics 35, 1741–1750.
| GDF-9 and BMP-15 direct the follicle symphony.Crossref | GoogleScholarGoogle Scholar | 30039232PubMed |
Satrapa RA, Nabhan T, Silva CF, Simões RAL, Razza EM, Puelker RZ, Trinca LA, Barros CM (2011) Influence of sire breed (Bos indicus versus Bos taurus) and interval from slaughter to oocyte aspiration on heat stress tolerance of in vitro-produced bovine embryos. Theriogenology 76, 1162–1167.
| Influence of sire breed (Bos indicus versus Bos taurus) and interval from slaughter to oocyte aspiration on heat stress tolerance of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 21783238PubMed |
Sdmit D, Niemann H (1999) Biotechnology in genetics and reproduction. Livestock Production Science 59, 207–221.
| Biotechnology in genetics and reproduction.Crossref | GoogleScholarGoogle Scholar |
Shi DS, Avery B, Greve T (1998) Effects of temperature gradients on in vitro maturation of bovine oocytes. Theriogenology 50, 667–674.
| Effects of temperature gradients on in vitro maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 10732157PubMed |
Shimasaki S (2006) BMP-15 regulation of ovulation quota in mammals. Reproductive Medicine and Biology 5, 245–248.
| BMP-15 regulation of ovulation quota in mammals.Crossref | GoogleScholarGoogle Scholar | 29699253PubMed |
Shimizu T, Yokoo M, Miyake Y, Sasada H, Sato E (2004) Differential expression of bone morphogenetic protein 4-6 (BMP-4, -5, and -6) and growth differentiation factor-9 (GDF-9) during ovarian development in neonatal pigs. Domestic Animal Endocrinology 27, 397–405.
| Differential expression of bone morphogenetic protein 4-6 (BMP-4, -5, and -6) and growth differentiation factor-9 (GDF-9) during ovarian development in neonatal pigs.Crossref | GoogleScholarGoogle Scholar | 15519042PubMed |
Sirard MA, Blondin P (1996) Oocyte maturation and IVF in cattle. Animal Reproduction Science 42, 417–426.
| Oocyte maturation and IVF in cattle.Crossref | GoogleScholarGoogle Scholar |
Sirard M-A, Coenen K (2006) In vitro maturation and embryo production in cattle. Methods in Molecular Biology 348, 35–42.
| In vitro maturation and embryo production in cattle.Crossref | GoogleScholarGoogle Scholar | 16988370PubMed |
Sirard M-A, Richard F, Blondin P, Robert C (2006) Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
| Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar | 16256189PubMed |
Smiljakovic T, Tomek W (2006) Meiotic maturation and in vitro maturation of bovine oocytes. Biotechnology in Animal Husbandry 22, 29–34.
| Meiotic maturation and in vitro maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Somfai T, Hirao Y (2021) Vitrification of immature bovine oocytes in protein-free media: the impact of the cryoprotectant treatment protocol, base medium, and ovary storage. Theriogenology 172, 47–54.
| Vitrification of immature bovine oocytes in protein-free media: the impact of the cryoprotectant treatment protocol, base medium, and ovary storage.Crossref | GoogleScholarGoogle Scholar | 34098168PubMed |
Sprícigo JFW, Sena Netto SB, Muterlle CV, Rodrigues SAD, Leme LO, Guimarães AL, Caixeta FMC, Franco MM, Pivato I, Dode MAN (2016) Intrafollicular transfer of fresh and vitrified immature bovine oocytes. Theriogenology 86, 2054–2062.
| Intrafollicular transfer of fresh and vitrified immature bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Stachecki JJ, Munné S, Cohen J (2004) Spindle organization after cryopreservation of mouse, human, and bovine oocytes. Reproductive BioMedicine Online 8, 664–672.
| Spindle organization after cryopreservation of mouse, human, and bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15169583PubMed |
Steller JG, Alberts JR, Ronca AE (2018) Oxidative stress as cause, consequence, or biomarker of altered female reproduction and development in the space environment. International Journal of Molecular Sciences 19, 3729
| Oxidative stress as cause, consequence, or biomarker of altered female reproduction and development in the space environment.Crossref | GoogleScholarGoogle Scholar |
Tanghe S, Van Soom A, Mehrzad J, Maes D, Duchateau L, de Kruif A (2003) Cumulus contributions during bovine fertilization in vitro. Theriogenology 60, 135–149.
| Cumulus contributions during bovine fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 12620587PubMed |
Thibault C, Szöllösi D, Gérard M (1987) Mammalian oocyte maturation. Reproduction Nutrition Développement 27, 865–896. https://hal.archives-ouvertes.fr/hal-00898700
Thomas RE, Armstrong DT, Gilchrist RB (2004) Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biology of Reproduction 70, 548–556.
| Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels.Crossref | GoogleScholarGoogle Scholar | 14568915PubMed |
Vieira AD, Forell F, Feltrin C, Rodrigues JL (2008) Calves born after direct transfer of vitrified bovine in vitro-produced blastocysts derived from vitrified immature oocytes. Reproduction in Domestic Animals 43, 314–318.
| Calves born after direct transfer of vitrified bovine in vitro-produced blastocysts derived from vitrified immature oocytes.Crossref | GoogleScholarGoogle Scholar | 18086255PubMed |
Vining LM, Zak LJ, Harvey SC, Harvey KE (2021) The role of apoptosis in cryopreserved animal oocytes and embryos. Theriogenology 173, 93–101.
| The role of apoptosis in cryopreserved animal oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 34365139PubMed |
Wang S, He G, Chen M, Zuo T, Xu W, Liu X (2017) The role of antioxidant enzymes in the ovaries. Oxidative Medicine and Cellular Longevity 2017, 4371714
| The role of antioxidant enzymes in the ovaries.Crossref | GoogleScholarGoogle Scholar | 29147461PubMed |
Zhu Y, Maric J, Nilsson M, Brännström M, Janson PO, Sundfeldt K (2004) Formation and barrier function of tight junctions in human ovarian surface epithelium. Biology of Reproduction 71, 53–59.
| Formation and barrier function of tight junctions in human ovarian surface epithelium.Crossref | GoogleScholarGoogle Scholar | 14973266PubMed |
