Scoping review of primary studies evaluating Bovine in vitro oocyte maturation and embryo development
Main Article Content
Abstract
We conducted a scoping review to 1) map and categorize published studies reporting interventions during the in vitro production of Bovine embryos and 2) qualitatively summarize the effects of treatments based on hormones, growth factors, sera, and reproductive fluids during oocyte maturation and embryo development. We searched electronic databases using keywords ('Bovine', 'embryo', 'blastocyst', 'oocyte', 'in vitro', 'quality') derived from the PIOS approach of the PRISMA statement. We identified 231 studies published during 2000−2021, with 133 being published between 2012 and 2021. The 231 studies were classified into four treatment categories: culture conditions (28), medium composition (45), bioactive supplements (79), and other additives (79), with 19 subcategories within these categories. A total of 77 studies included hormones, growth factors, sera, and reproductive fluids, among which 53 studies reported a positive effect on embryo production. Hormone-based treatments using melatonin, gonadotropins, and steroids were the most effective, followed by interventions assessing growth factors such as EGF, FGF, IGF-1, and BMP. These treatments improved oocyte competence, cytoplasmic/nuclear maturation, oocyte quality, and blastocyst development. Although free-serum media and synthetic/alternative products can partially or totally replace serum, it is sometimes necessary even at low concentrations. At high concentrations, hormones or growth factors may have detrimental effects on oocyte nuclear maturation, impair embryo development, and decrease embryo survival. Further meta-analyses are needed to estimate the intervention-specific effects. Future research should focus on interventions that have a positive effect and can be used extensively for Bovine production.
Article Details
References
Galli C, Duchi R, Crotti G, Turini P, Ponderato N, Colleoni S, et al. Bovine embryo technologies. Theriogenology. 2003;59(2):599−616. doi: 10.1016/s0093-691x(02)01243-8.
Galli C, Lazzari G. Practical aspects of IVM/IVF in cattle. Animal reproduction science. 1996;42(1−4):371−379.
Ferré L, Kjelland M, Strøbech L, Hyttel P, Mermillod P, Ross P. Recent advances in Bovine in vitro embryo production: reproductive biotechnology history and methods. Animal. 2020;14(5):991−1004. doi: 10.1017/S1751731119002775.
Wooldridge LK, Keane JA, Rhoads ML, Ealy AD. Bioactive supplements influencing Bovine in vitro embryo development. Journal of Animal Science. 2022;100(7):skac091. doi: 10.1093/jas/skac091.
Nikoloff N, Pascua AM, Anchordoquy JM, Anchordoquy JP, Sirini MA, Seoane A, Furnus CC. Effect of eicosapentaenoic acid on Bovine cumulus–oocyte complex in vitro. Cell Biology International. 2017;41(5):505−513. doi: 10.1002/cbin.10746.
Crosier AE, Farin PW, Dykstra MJ, Alexander JE, Farin CE. Ultrastructural morphometry of Bovine blastocysts produced in vivo or in vitro. Biology of Reproduction. 2001;64(5):1375−1385. doi: 10.1095/biolreprod64.5.1375.
Hansen P. Realizing the promise of IVF in cattle-an overview. Theriogenology. 2006;65(1):119−125. doi: 10.1016/j.theriogenology.2005.09.019.
Perkel KJ, Tscherner A, Merrill C, Lamarre J, Madan P. The ART of selecting the best embryo: a review of early embryonic mortality and Bovine embryo viability assessment methods. Molecular reproduction and development. 2015;82(11):822−838. doi: 10.1002/mrd.22525.
Bó G, Mapletoft R. Evaluation and classification of Bovine embryos. Animal Reproduction. 2018;10(3):344−348.
Charpigny G, Marquant-Le Guienne B, Richard C, Adenot P, Dubois O, Gelin V, et al. PGE2 supplementation of oocyte culture media improves the developmental and cryotolerance performance of Bovine blastocysts derived from a serum-free in vitro production system, mirroring the inner cell mass transcriptome. Frontiers in Cell and Developmental Biology. 2021;9:20. doi: 10.3389/fcell.2021.672948.
Kowalczyk-Zieba I, Boruszewska D, Suwik K, Staszkiewicz-Chodor J, Jaworska J, Woclawek-Potocka I. Iloprost affects in vitro maturation and developmental competence of Bovine oocytes. Theriogenology. 2020;157:286−296. doi: 10.1016/j.theriogenology.2020.07.035.
Canon-Beltran K, Cajas YN, Perez-Cerezales S, Leal CLV, Agirregoitia E, Gutierrez-Adan A, et al. Nobiletin enhances the development and quality of Bovine embryos in vitro during two key periods of embryonic genome activation. Scientific Reports. 2021;11(1):18. doi: 10.1038/s41598-021-91158-7.
Sirard M-A, Richard F, Blondin P, Robert C. Contribution of the oocyte to embryo quality. Theriogenology. 2006;65(1):126−136. doi: 10.1016/j.theriogenology.2005.09.020.
Arksey H, O'Malley L. Scoping studies: towards a methodological framework. International journal of social research methodology. 2005;8(1):19−32. doi: 10.1080/1364557032000119616.
Diaz D, Lopez-Orrantia AM, Camacho AN, Rosiles RJ, Rodriguez-Gaxiola MA, Romo-Rubio JA, et al. A scoping review and systematic map of primary studies assessing heat stress on reproductive, physiological, and productive parameters of farm animals. Veterinaria México OA. 2022;9. doi: 10.22201/fmvz.24486760e.2022.1121.
Rubio-Rocha YG, Gaxiola SM, Chávez C, Ceballos G, Bojorquez C, Diaz D. Jaguar (Panthera onca) food resource use and its interaction with humans: scoping review. Veterinaria México OA. 2023;10. doi: 10.22201/fmvz.24486760e.2023.1107.
Colquhoun HL, Levac D, O'Brien KK, Straus S, Tricco AC, Perrier L, et al. Scoping reviews: time for clarity in definition, methods, and reporting. Journal of clinical epidemiology. 2014;67(12):1291−1294. doi: 10.1016/j.jclinepi.2014.03.013.
Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): checklist and explanation. Annals of Internal Medicine. 2018;169(7):467−473. doi: 10.7326/m18-0850.
Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic reviews. 2015;4(1):1. doi: 0.1186/2046-4053-4-1.
Van Driel ML, De Sutter A, De Maeseneer J, Christiaens T. Searching for unpublished trials in Cochrane reviews may not be worth the effort. Journal of clinical epidemiology. 2009;62(8):838−844. e833. doi: 10.1016/j.jclinepi.2008.09.010.
Viana J. 2019 Statistics of embryo production and transfer in domestic farm animals. Diverging trends for IVD and IVP embryos. Embryo Technology Newsletter. 2020:17.
Han KW, Chun JL, Lee JH, Kim KJ, Lee KB, Gotoh T, et al. Co-culture with amniotic membrane stem cells for oocyte maturation and early embryonic eevelopment in Bovine. Journal of the Faculty of Agriculture Kyushu University. 2015;60(2):393−398. doi: 10.5109/1526400.
Imai K, Matoba S, Dochi O, Shimohira I. Different factors affect developmental competence and cryotolerance in in vitro produced Bovine embryo. J Vet Med Sci. 2002;64(10):887−891. doi: 10.1292/jvms.64.887.
Cordova A, Perreau C, Uzbekova S, Ponsart C, Locatelli Y, Mermillod P. Development rate and gene expression of IVP Bovine embryos cocultured with Bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology. 2014;81(9):1163−1173. doi: 10.1016/j.theriogenology.2014.01.012.
Opiela J, Bülbül B, Romanek J. Varied approach of using MSCs for Bovine embryo in vitro culture. Animal Biotechnology. 2020;31(1):1−8. doi: 10.1080/10495398.2018.1448224.
Pereira DM, Cardoso CJT, da Silva WAL, Souza-Cáceres MB, Santos M, Pöhland R, et al. Production of in vitro Bovine embryos supplemented with L-carnitine in different oxygen tensions and the relation to nitric oxide. Zygote. 2020;28(5):403−408. doi: 10.1017/S0967199420000258.
Correa GA, Rumpf R, Mundim TCD, Franco MM, Dode MAN. Oxygen tension during in vitro culture of Bovine embryos: effect in production and expression of genes related to oxidative stress. Animal Reproduction Science. 2008;104(2−4):132−142. doi: 10.1016/j.anireprosci.2007.02.002.
Matta S, Caldas-Bussiere M, Viana K, Faes M, de Carvalho CP, Dias B, Quirino C. Effect of inhibition of synthesis of inducible nitric oxide synthase-derived nitric oxide by aminoguanidine on the in vitro maturation of oocyte–cumulus complexes of cattle. Animal Reproduction Science. 2009;111(2−4):189−201. doi: 10.1016/j.anireprosci.2008.03.002.
Gopichandran N, Leese HJ. The effect of paracrine/autocrine interactions on the in vitro culture of Bovine preimplantation embryos. Reproduction. 2006;131(2):269−277. doi: 10.1530/rep.1.00677.
Azari-Dolatabad N, Raes A, Pavani KC, Asaadi A, Angel-Velez D, van Damme P, et al. Follicular fluid during individual oocyte maturation enhances cumulus expansion and improves embryo development and quality in a dose-specific manner. Theriogenology. 2021;166:38−45. doi: 10.1016/j.theriogenology.2021.02.016.
Ahumada CJ, Salvador I, Cebrian-Serrano A, Lopera R, Silvestre MA. Effect of supplementation of different growth factors in embryo culture medium with a small number of Bovine embryos on in vitro embryo development and quality. Animal. 2013;7(3):455−462. doi: 10.1017/S1751731112001991.
Cebrian-Serrano A, Salvador I, Silvestre MA. Beneficial effect of two culture systems with small groups of embryos on the development and quality of in vitro-produced Bovine embryos. Anat Histol Embryol. 2014;43(1):22−30. doi: 10.1111/ahe.12043.
Sirard MA. Factors affecting oocyte and embryo transcriptomes. Reproduction in Domestic Animals. 2012;47:148−155. doi: 10.1111/j.1439-0531.2012.02069.x.
Mucci N, Aller J, Kaiser GG, Hozbor F, Cabodevila J, Alberio RH. Effect of estrous cow serum during Bovine embryo culture on blastocyst development and cryotolerance after slow freezing or vitrification. Theriogenology. 2006;65(8):1551−1562. doi: 10.1016/j.theriogenology.2005.08.020.
Restrepo G, Chavarría N, Vásquez NA. Efecto de la suplementación con suero fetal bovino para la maduración in vitro de oocitos bovinos sobre su actividad mitocondrial y desarrollo embrionario. Revista CES Medicina Veterinaria y Zootecnia. 2007;2(2):14−22.
Hamdi M, Lopera-Vasquez R, Maillo V, Sanchez-Calabuig MJ, Nunez C, Gutierrez-Adan A, Rizos D. Bovine oviductal and uterine fluid support in vitro embryo development. Reproduction Fertility and Development. 2018;30(7):935−945. doi: 10.1071/RD17286.
Gandhi AP, Lane M, Gardner DK, Krisher RL. A single medium supports development of Bovine embryos throughout maturation, fertilization and culture. Hum Reprod. 2000;15(2):395−401. doi: 10.1093/humrep/15.2.395.
Cevİk M, Kocygit A, Sen U, Kuran M. Can sequential human embryo culture media be used in Bovine in vitro embryo culture? Kafkas Universitesi Veteriner Fakultesi Dergisi. 2014;20(1):149−153. doi: 10.9775/kvfd.2013.9676.
Duque P, Gómez E, Dı́az E, Facal N, Hidalgo C, Dı́ez C. Use of two replacements of serum during Bovine embryo culture in vitro. Theriogenology. 2003;59(3−4):889−899. doi: 10.1016/s0093-691x(02)01134-2.
George F, Daniaux C, Genicot G, Verhaeghe B, Lambert P, Donnay I. Set up of a serum-free culture system for Bovine embryos: embryo development and quality before and after transient transfer. Theriogenology. 2008;69(5):612−623. doi: 10.1016/j.theriogenology.2007.11.008.
Palasz AT, Beltran Brena P, De la Fuente J, Gutierrez-Adan A. The effect of Bovine embryo culture without proteins supplements until day 4 on transcription level of hyaluronan synthases, receptors and mtDNA content. Zygote. 2010;18(2):121−129. doi: 10.1017/S0967199409990128.
Maurer H. Towards serum-free, chemically defined media for mammalian cell culture. Animal cell culture: a practical approach. 1992.
Sung LY, Du F, Xu J, Chang W, Nedambale TL, Zhang J, et al. The differential requirement of albumin and sodium citrate on the development of in vitro produced Bovine embryos. Reprod Nutr Dev. 2004;44(6):551−564. doi: 10.1051/rnd:2004061.
Moreno D, Neira A, Dubreil L, Liegeois L, Destrumelle S, Michaud S, et al. In vitro Bovine embryo production in a synthetic medium: embryo development, cryosurvival, and establishment of pregnancy. Theriogenology. 2015;84(7):1053−1060. doi: 10.1016/j.theriogenology.2015.04.014.
Del Collado M, Saraiva NZ, Lopes FL, Cruz MH, Gaspar RC, Oliveira CS, et al. Efeitos da redução ou substituição do soro fetal bovino por outros compostos na maturação in vitro de oócitos bovinos. Pesquisa Veterinária Brasileira. 2014;34(7):689−694. doi: 10.1590/s0100-736x2014000700014.
Lim KT, Jang G, Ko KH, Lee WW, Park HJ, Kim JJ, et al. Improved in vitro Bovine embryo development and increased efficiency in producing viable calves using defined media. Theriogenology. 2007;67(2):293−302. doi: 10.1016/j.theriogenology.2006.07.011.
Sagirkaya H, Yagmur M, Nur Z, Soylu MK. Replacement of fetal calf serum with synthetic serum substitute in the in vitro maturation medium: effects on maturation, fertilization and subsequent development of cattle oocytes in vitro. Turkish Journal of Veterinary & Animal Sciences. 2004;28(4):779−784.
Sagirkaya H, Misirlioglu M, Kaya A, First NL, Parrish JJ, Memili E. Developmental potential of Bovine oocytes cultured in different maturation and culture conditions. Anim Reprod Sci. 2007;101(3−4):225−240. doi: 10.1016/j.anireprosci.2006.09.016.
Marei WF, Ghafari F, Fouladi-Nashta AA. Role of hyaluronic acid in maturation and further early embryo development of Bovine oocytes. Theriogenology. 2012;78(3):670−677. doi: 10.1016/j.theriogenology.2012.03.013.
Opiela J, Latasiewicz E, Smorag Z. Optimal concentration of hyaluronan and plant protein in different culture systems for in vitro maturation of Bovine oocytes. Indian J Exp Biol. 2012;50(12):839−846. PMID: 23986966.
Palasz AT, Brena PB, Martinez MF, Perez-Garnelo SS, Ramirez MA, Gutierrez-Adan A, de la Fuente J. Development, molecular composition and freeze tolerance of Bovine embryos cultured in TCM-199 supplemented with hyaluronan. Zygote. 2008;16(1):39−47. doi: 10.1017/S0967199407004467.
Stojkovic M, Kolle S, Peinl S, Stojkovic P, Zakhartchenko V, Thompson JG, et al. Effects of high concentrations of hyaluronan in culture medium on development and survival rates of fresh and frozen-thawed Bovine embryos produced in vitro. Reproduction. 2002;124(1):141−153. doi: 10.1530/rep.0.1240141.
Rodrigues SAD, Pontelo TP, Kussano NR, Kawamoto TS, Leme LO, Caixeta FMC, et al. Effects of prostaglandins E2 and F2alpha on the in vitro maturation of Bovine oocytes. Domestic Animal Endocrinology. 2020;72:106447. doi: 10.1016/j.domaniend.2020.106447.
Marques TC, da Silva Santos EC, Diesel TO, Martins CF, Cumpa HCB, de Oliveira Leme L, et al. Blastocoel fluid removal and melatonin supplementation in the culture medium improve the viability of vitrified Bovine embryos. Theriogenology. 2021;160:134−141. doi: 10.1016/j.theriogenology.2020.10.028.
Marques T, da Silva Santos E, Diesel T, Leme L, Martins C, Dode M, et al. Melatonin reduces apoptotic cells, SOD 2 and HSPB 1 and improves the in vitro production and quality of Bovine blastocysts. Reproduction in Domestic Animals. 2018;53(1):226−236. doi: 10.1111/rda.13097.
Diogenes MN, Guimaraes AL, Leme LO, Dode MA. Bovine in vitro embryo production: the effects of fibroblast growth factor 10 (FGF10). Journal of Assisted Reproduction and Genetics. 2017;34(3):383−390. doi: 10.1007/s10815-016-0852-8.
Carrillo-Gonzalez DF, Maldonado-Estrada JG. L-carnitine supplementation in culture media improves the pregnancy rate of in vitro produced embryos with sexed semen from Bos taurus indicus cows. Tropical Animal Health and Production. 2020;52(5):2559−2565. doi: 10.1007/s11250-020-02281-y.
Ali A, Sirard MA. Protein kinases influence Bovine oocyte competence during short-term treatment with recombinant human follicle stimulating hormone. Reproduction. 2005;130(3):303−310. doi: 10.1530/rep.1.00387.
Choi YH, Carnevale EM, Seidel GE Jr., Squire EL. Effects of gonadotropins on Bovine oocytes matured in TCM-199. Theriogenology. 2001;56(4):661−670. doi: 10.1016/s0093-691x(01)00597-0.
Liu S, Feng HL, Marchesi D, Chen ZJ, Hershlag A. Dose-dependent effects of gonadotropin on oocyte developmental competence and apoptosis. Reproduction Fertility and Development. 2011;23(8):990−996. doi: 10.1071/RD11079.
Salgado R, Vergara G Ó, Ramírez P L. Efecto de gonadotropinas sobre la maduración y desarrollo embrionario de oocitos bovinos cultivados in vitro. Revista MVZ Córdoba. 2010;15(1):1954−1960. doi: 10.21897/rmvz.333.
Kaya A, Sairkaya H, Misirliolu M, Gümen A, Parrish JJ, Memili E. Leptin and IGF-I improve Bovine embryo quality in vitro. Animal Reproduction. 2017;14(4):1151−1160. doi: 10.21451/1984-3143-ar987.
Boelhauve M, Sinowatz F, Wolf E, Paula-Lopes FF. Maturation of Bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biology of Reproduction. 2005;73(4):737−744. doi: 10.1095/biolreprod.105.041103.
Jia Z, Zhang J, Wu Z, Tian J. Leptin enhances maturation and development of calf oocytes in vitro. Reproduction in Domestic Animals. 2012;47(5):718−723. doi: 10.1111/j.1439-0531.2011.01949.x.
Arias-Alvarez M, Bermejo-Alvarez P, Gutierrez-Adan A, Rizos D, Lorenzo PL, Lonergan P. Effect of leptin supplementation during in vitro oocyte maturation and embryo culture on Bovine embryo development and gene expression patterns. Theriogenology. 2011;75(5):887−896. doi: 10.1016/j.theriogenology.2010.10.031.
da Costa NN, Brito KN, Santana P, Cordeiro Mda S, Silva TV, Santos AX, et al. Effect of cortisol on Bovine oocyte maturation and embryo development in vitro. Theriogenology. 2016;85(2):323−329. doi: 10.1016/j.theriogenology.2015.08.010.
Banliat C, Dubuisson F, Corbin E, Beurois J, Tomas D, Le Bourhis D, et al. Intraoviductal concentrations of steroid hormones during in vitro culture changed phospholipid profiles and cryotolerance of Bovine embryos. Molecular Reproduction and Development. 2019;86(6):661−672. doi: 10.1002/mrd.23144.
Costa NN, Cordeiro MS, Silva TV, Sastre D, Santana PP, Sa AL, et al. Effect of triiodothyronine on developmental competence of Bovine oocytes. Theriogenology. 2013;80(4):295−301. doi: 10.1016/j.theriogenology.2013.04.011.
Ashkar FA, Semple E, Schmidt CH, St John E, Bartlewski PM, King WA. Thyroid hormone supplementation improves Bovine embryo development in vitro. Human Reproduction. 2010;25(2):334−344. doi: 10.1093/humrep/dep394.
Dong YJ, Varisanga MD, Mtango NR, Aono M, Otoi T, Suzuki T. Improvement of the culture conditions for in vitro production of cattle embryos in a portable CO2 incubator. Reproduction in Domestic Animals. 2001;36(6):313−318. doi: 10.1046/j.1439-0531.2001.00308.x.
Moreira F, Paula-Lopes FF, Hansen PJ, Badinga L, Thatcher WW. Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived Bovine embryos. Theriogenology. 2002;57(2):895−907. doi: 10.1016/s0093-691x(01)00694-x.
Iwata H, Ohota M, Hashimoto S, Kimura K, Isaji M, Miyake M. Stage-specific effect of growth hormone on developmental competence of Bovine embryos produced in vitro. Journal of Reproduction and Development. 2003;49(6):493−499. doi: 10.1262/jrd.49.493.
Dovolou E, Messinis IE, Periquesta E, Dafopoulos K, Gutierrez-Adan A, Amiridis GS. Ghrelin accelerates in vitro maturation of Bovine oocytes. Reproduction in Domestic Animals. 2014;49(4):665−672. doi: 10.1111/rda.12344.
Dovolou E, Periquesta E, Messinis IE, Tsiligianni T, Dafopoulos K, Gutierrez-Adan A, Amiridis GS. Daily supplementation with ghrelin improves in vitro Bovine blastocysts formation rate and alters gene expression related to embryo quality. Theriogenology. 2014;81(4):565−571. doi: 10.1016/j.theriogenology.2013.11.009.
Dashtizad M, Haron AW, Yusoff R, Daliri M, Hajarian H, Najari M, et al. Synergistic effect of insulin on in vitro development of immature Bovine oocytes. American Journal of Animal and Veterinary Sciences. 2010;5(4):258−265. doi: 10.3844/ajavsp.2010.258.265.
Beker AR, Colenbrander B, Bevers MM. Effect of 17beta-estradiol on the in vitro maturation of Bovine oocytes. Theriogenology. 2002;58(9):1663−1673. doi: 10.1016/s0093-691x(02)01082-8.
Larson JE, Krisher RL, Lamb GC. Effects of supplemental progesterone on the development, metabolism and blastocyst cell number of Bovine embryos produced in vitro. Reproduction Fertility and Development. 2011;23(2):311−318. doi: 10.1071/RD10106.
Matsuo M, Sumitomo K, Ogino C, Gunji Y, Nishimura R, Hishinuma M. Three-step in vitro maturation culture of Bovine oocytes imitating temporal changes of estradiol-17<i>β</i> and progesterone concentrations in preovulatory follicular fluid. Archives Animal Breeding. 2017;60(4):385−390. doi: 10.5194/aab-60-385-2017.
Reis AN, Silva LKX, Silva AOA, Sousa JS, Vale WG. Effect of estradiol and progesterone on development and quality of Bovine embryos produced in vitro. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2010;62(6):1375−1380. doi: 10.1590/s0102-09352010000600012.
Silva CC, Knight PG. Effects of androgens, progesterone and their antagonists on the developmental competence of in vitro matured Bovine oocytes. Journal of Reproduction and Fertility. 2000;119(2):261−269. PMID: 10864838
Soares ACS, Lodde V, Barros RG, Price CA, Luciano AM, Buratini J. Steroid hormones interact with natriuretic peptide C to delay nuclear maturation, to maintain oocyte-cumulus communication and to improve the quality of in vitro-produced embryos in cattle. Reproduction Fertility and Development. 2017;29(11):2217−2224. doi: 10.1071/RD16320.
Marques TC, Santos E, Diesel TO, Martins CF, Cumpa HCB, Leme LO, et al. Blastocoel fluid removal and melatonin supplementation in the culture medium improve the viability of vitrified Bovine embryos. Theriogenology. 2021;160:134−141. doi: 10.1016/j.theriogenology.2020.10.028.
Zhao XM, Wang N, Hao HS, Li CY, Zhao YH, Yan CL, et al. Melatonin improves the fertilization capacity and developmental ability of Bovine oocytes by regulating cytoplasmic maturation events. J Pineal Res. 2018;64(1):15. doi: 10.1111/jpi.12445.
Wang F, Tian X, Zhou Y, Tan D, Zhu S, Dai Y, Liu G. Melatonin improves the quality of in vitro produced (IVP) Bovine embryos: implications for blastocyst development, cryotolerance, and modifications of relevant gene expression. PloS one. 2014;9(4):e93641. doi: 10.1371/journal.pone.0093641.
Yang M, Tao J, Chai M, Wu H, Wang J, Li G, et al. Melatonin improves the quality of inferior Bovine oocytes and promoted their subsequent IVF embryo development: mechanisms and results. Molecules. 2017;22(12):15. doi: 10.3390/molecules22122059.
Marques TC, da Silva Santos EC, Diesel TO, Leme LO, Martins CF, Dode M, et al. Melatonin reduces apoptotic cells, SOD2 and HSPB1 and improves the in vitro production and quality of Bovine blastocysts. Reproduction in Domestic Animals. 2018;53(1):226−236. doi: 10.1111/rda.13097.
Pang Y, Zhao S, Sun Y, Jiang X, Hao H, Du W, Zhu H. Protective effects of melatonin on the in vitro developmental competence of Bovine oocytes. Animal Science Journal. 2018;89(4):648−660. doi: 10.1111/asj.12970.
Tian X, Wang F, He C, Zhang L, Tan D, Reiter RJ, et al. Beneficial effects of melatonin on Bovine oocytes maturation: a mechanistic approach. Journal of Pineal Research. 2014;57(3):239−247. doi: 10.1111/jpi.12163.
Gutierrez-Anez JC, Lucas-Hahn A, Hadeler KG, Aldag P, Niemann H. Melatonin enhances in vitro developmental competence of cumulus-oocyte complexes collected by ovum pick-up in prepubertal and adult dairy cattle. Theriogenology. 2021;161:285−293. doi: 10.1016/j.theriogenology.2020.12.011.
Algarra B, Maillo V, Aviles M, Gutierrez-Adan A, Rizos D, Jimenez-Movilla M. Effects of recombinant OVGP1 protein on in vitro Bovine embryo development. Journal of Reproduction and Development. 2018;64(5):433−443. doi: 10.1262/jrd.2018-058.
Yoshioka K, Suzuki C, Iwamura S. Effects of activin A and follistatin on developmental kinetics of Bovine embryos: cinematographic analysis in a chemically defined medium. Journal of Reproduction and Fertility. 2000;118(1):119−125. doi: 10.1530/reprod/118.1.119.
Sakagami N, Umeki H, Nishino O, Uchiyama H, Ichikawa K, Takeshita K, et al. Normal calves produced after transfer of embryos cultured in a chemically defined medium supplemented with epidermal growth factor and insulin-like growth factor I following ovum pick up and in vitro fertilization in Japanese black cows. J Reprod Dev. 2012;58(1):140−146. doi: 10.1262/jrd.11-050m.
Sirisathien S, Brackett BG. TUNEL analyses of Bovine blastocysts after culture with EGF and IGF-I. Mol Reprod Dev. 2003;65(1):51−56. doi: 10.1002/mrd.10263.
Sirisathien S, Hernandez-Fonseca HJ, Brackett BG. Influences of epidermal growth factor and insulin-like growth factor-I on Bovine blastocyst development in vitro. Anim Reprod Sci. 2003;77(1−2):21−32. doi: 10.1016/s0378-4320(02)00272-5.
Mesalam A, Lee KL, Khan I, Chowdhury MMR, Zhang S, Song SH, et al. A combination of Bovine serum albumin with insulin-transferrin-sodium selenite and/or epidermal growth factor as alternatives to fetal Bovine serum in culture medium improves Bovine embryo quality and trophoblast invasion by induction of matrix metalloproteinases. Reprod Fertil Dev. 2019;31(2):333−346. doi: 10.1071/RD18162.
Mtango NR, Varisanga MD, Dong YJ, Rajamahendran R, Suzuki T. Growth factors and growth hormone enhance in vitro embryo production and post-thaw survival of vitrified Bovine blastocysts. Theriogenology. 2003;59(5−6):1393−1402. doi: 10.1016/s0093-691x(02)01163-9.
Polat B, Salmanoglu MR. The influence of epidermal growth factor on maturation and fertilisation of Bovine oocytes in vitro. Turkish Journal of Veterinary & Animal Sciences. 2008;32(6):457−462.
Wang Z, Fu C, Yu S. Effects of green tea polyphenols, insulin-like growth factor I and glucose on developmental competence of Bovine oocytes. Revista Brasileira de Zootecnia. 2012;41(12):2418−2423. doi: 10.1590/s1516-35982012001200006.
Neira JA, Tainturier D, Pena MA, Martal J. Effect of the association of IGF-I, IGF-II, bFGF, TGF-beta1, GM-CSF, and LIF on the development of Bovine embryos produced in vitro. Theriogenology. 2010;73(5):595−604. doi: 10.1016/j.theriogenology.2009.10.015.
Kocygit A, Cevik M, Sen U, Kuran M. The effect of macromolecule and growth factor combinations on in vitrodevelopment of Bovine embryos. Turkish Journal of Veterinary and Animal Sciences. 2015;39(3):308−313. doi: 10.3906/vet-1411−1445.
Hernandez-Fonseca HJ, Sirisathien S, Bosch P, Cho HS, Lott JD, Hawkins LL, et al. Offspring resulting from direct transfer of cryopreserved Bovine embryos produced in vitro in chemically defined media. Animal Reproduction Science. 2002;69(3−4):151−158. doi: 10.1016/s0378-4320(01)00178-6.
Velazquez MA, Hermann D, Kues WA, Niemann H. Increased apoptosis in Bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor. Reproduction. 2011;141(1):91−103. doi: 10.1530/REP-10-0336.
Dhali A, Anchamparuthy VM, Butler SP, Pearson RE, Gwazdauskas FC. In vitro development of Bovine embryos cultured with stem cell factor or insulin-like growth factor-I following IVF with semen of two bulls having different field fertility. Anim Reprod Sci. 2009;116(3−4):188−195. doi: 10.1016/j.anireprosci.2009.02.007.
Zhang K, Ealy AD. Supplementing fibroblast growth factor 2 during Bovine oocyte <i>in vitro</i> maturation promotes subsequent embryonic development. Open Journal of Animal Sciences. 2012;02(02):119−126. doi: 10.4236/ojas.2012.22017.
Fields SD, Hansen PJ, Ealy AD. Fibroblast growth factor requirements for in vitro development of Bovine embryos. Theriogenology. 2011;75(8):1466−1475. doi: 10.1016/j.theriogenology.2010.12.007.
Diogenes MN, Guimaraes ALS, Leme LO, Mauricio MF, Dode MAN. Effect of prematuration and maturation with fibroblast growth factor 10 (FGF10) on in vitro development of Bovine oocytes. Theriogenology. 2017;102:190−198. doi: 10.1016/j.theriogenology.2017.06.004.
Machado MF, Caixeta ES, Sudiman J, Gilchrist RB, Thompson JG, Lima PF, et al. Fibroblast growth factor 17 and bone morphogenetic protein 15 enhance cumulus expansion and improve quality of in vitro-produced embryos in cattle. Theriogenology. 2015;84(3):390−398. doi: 10.1016/j.theriogenology.2015.03.031.
Sudiman J, Sutton-McDowall ML, Ritter LJ, White MA, Mottershead DG, Thompson JG, Gilchrist RB. Bone morphogenetic protein 15 in the pro-mature complex form enhances Bovine oocyte developmental competence. PloS One. 2014;9(7):e103563. doi: 10.1371/journal.pone.0103563.
Sugimura S, Ritter LJ, Sutton-McDowall ML, Mottershead DG, Thompson JG, Gilchrist RB. Amphiregulin co-operates with bone morphogenetic protein 15 to increase Bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. Mol Hum Reprod. 2014;20(6):499−513. doi: 10.1093/molehr/gau013.
Conde P, Morado S, Alvarez G, Smitz J, Gentile T, Cetica P. Effect of the hematopoietic growth factors erythropoietin and kit ligand on Bovine oocyte in vitro maturation and developmental competence. Theriogenology. 2019;123:37−44. doi: 10.1016/j.theriogenology.2018.09.014.
Garcia-Hernandez J, Castro-Valenzuela BE, Rodriguez-Borbon A, Grado-Ahuir JA, Burrola-Barraza ME. IMD/ADM21-47, a factor that improves embryo quality. Theriogenology. 2020;146:1−13. doi: 10.1016/j.theriogenology.2020.01.049.
Salgado R, Barrera J, Correa S, Estrada L. Efecto de tres diferentes fracciones de peso molecular alto del medio condicionado por células BRL en el desarrollo embrionario bovino in vitro. Revista MVZ Córdoba. 2001;6(2):111−118.
Seekford ZK, Wooldridge LK, Dias NW, Timlin CL, Sales AF, Speckhart SL, et al. Interleukin-6 supplementation improves post-transfer embryonic and fetal development of in vitro-produced Bovine embryos. Theriogenology. 2021;170:15−22. doi: 10.1016/j.theriogenology.2021.04.004.
Vejlsted M, Avery B, Gjorret JO, Maddox-Hyttel P. Effect of leukemia inhibitory factor (LIF) on in vitro produced Bovine embryos and their outgrowth colonies. Mol Reprod Dev. 2005;70(4):445−454. doi: 10.1002/mrd.20221.
Collares LF, Pradieé J, Borges MA, Mion B, Gindri P, Fadrique J, et al. Supplementation of in vitro maturation medium with serum from dairy cows at early and late lactation in the in vitro production of Bovine embryos. Medicina Veterinária (UFRPE). 2018;12(4):311−315. doi: 10.26605/medvet-v12n4-2462.
Pereira MM, Machado MA, Costa FQ, Serapiao RV, Viana JH, Camargo LS. Effect of oxygen tension and serum during IVM on developmental competence of Bovine oocytes. Reprod Fertil Dev. 2010;22(7):1074−1082. doi: 10.1071/RD10007.
Fernandes-Franca PH, Oliveira-Santos MV, Oliveira-Lira GP, Azevedo-Borges A, Fernandes-Pereira A. Influence of different protein supplements on the recovery and in vitro maturation of Bovine oocytes. Revista Colombiana de Ciencias Pecuarias. 2019;33(3):172−181. doi: 10.17533/udea.rccp.v33n3a01.
Mesalam A, Kong R, Khan I, Chowdhury M, Choi BH, Kim SW, et al. Effect of charcoal:dextran stripped fetal Bovine serum on in vitro development of Bovine embryos. Reprod Biol. 2017;17(4):312−319. doi: 10.1016/j.repbio.2017.09.002.
Sudano MJ, Paschoal DM, Rascado Tda S, Magalhaes LC, Crocomo LF, de Lima-Neto JF, Landim-Alvarenga Fda C. Lipid content and apoptosis of in vitro-produced Bovine embryos as determinants of susceptibility to vitrification. Theriogenology. 2011;75(7):1211−1220. doi: 10.1016/j.theriogenology.2010.11.033.
Leivas FG, Brum DS, Fialho SS, Saliba WP, Alvim MT, Bernardi ML, et al. Fetal calf serum enhances in vitro production of Bos taurus indicus embryos. Theriogenology. 2011;75(3):429−433. doi: 10.1016/j.theriogenology.2010.08.017.
Reis A, Rooke JA, McCallum GJ, Staines ME, Ewen M, Lomax MA, McEvoy TG. Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of Bovine blastocysts produced in vitro. Reprod Fertil Dev. 2003;15(5):275−284. doi: 10.1071/rd03004.
Murillo A, Munoz M, Martin-Gonzalez D, Carrocera S, Martinez-Nistal A, Gomez E. Low serum concentration in Bovine embryo culture enhances early blastocyst rates on day-6 with quality traits in the expanded blastocyst stage similar to BSA-cultured embryos. Reprod Biol. 2017;17(2):162−171. doi: 10.1016/j.repbio.2017.04.002.
Alm H, Torner H, Kanitz W, Roschlau K. Influence of oocyte recovery method, in vitro fertilization method and serum source on embryonic development of in vitro matured Bovine oocytes. Archiv Fur Tierzucht-Archives of Animal Breeding. 2008;51(3):224−234. doi: 10.5194/aab-51-224-2008.
Caínzos J, Barrio M, Ruibal S, Becerra JJ, Quintela LA, Herradón PG. Effect of fetal calf serum (FCS), Bovine albumin serum (BSA) and polyvinyl pyrrolidone (PVP) suplementation in Bovine oocyte maturation medium in vitro. ITEA. 2013;109(1):25−32.
Ali A, Coenen K, Bousquet D, Sirard MA. Origin of Bovine follicular fluid and its effect during in vitro maturation on the developmental competence of Bovine oocytes. Theriogenology. 2004;62(9):1596−1606. doi: 10.1016/j.theriogenology.2004.03.011.
Momozawa K, Fukuda Y. Effects of fractions of Bovine follicular fluid and fetal Bovine serum as supplements to maturation medium on in vitro development of in vitro fertilized Bovine embryos. Journal of Mammalian Ova Research. 2011;28(1):68−74. doi: 10.1274/jmor.28.68.
Cruz MHC, Saraiva NZ, Cruz JFd, Oliveira CS, del Collado M, Fernandes H, et al. Effect of follicular fluid supplementation during in vitro maturation on total cell number in Bovine blastocysts produced in vitro. Revista Brasileira de Zootecnia. 2014;43(3):120−126. doi: 10.1590/s1516-35982014000300003.
Lopera-Vasquez R, Hamdi M, Maillo V, Lloreda V, Coy P, Gutierrez-Adan A, et al. Effect of Bovine oviductal fluid on development and quality of Bovine embryos produced in vitro. Reprod Fertil Dev. 2017;29(3):621−629. doi: 10.1071/RD15238.
Cebrian-Serrano A, Salvador I, Garcia-Rosello E, Pericuesta E, Perez-Cerezales S, Gutierrez-Adan A, et al. Effect of the Bovine oviductal fluid on in vitro fertilization, development and gene expression of in vitro-produced Bovine blastocysts. Reprod Domest Anim. 2013;48(2):331−338. doi: 10.1111/j.1439-0531.2012.02157.x.
License
Veterinaria México OA by Facultad de Medicina Veterinaria y Zootecnia - Universidad Nacional Autónoma de México is licensed under a Creative Commons Attribution 4.0 International Licence.
Based on a work at http://www.revistas.unam.mx
- All articles in Veterinaria México OA re published under the Creative Commons Attribution 4.0 Unported (CC-BY 4.0). With this license, authors retain copyright but allow any user to share, copy, distribute, transmit, adapt and make commercial use of the work, without needing to provide additional permission as long as appropriate attribution is made to the original author or source.
- By using this license, all Veterinaria México OAarticles meet or exceed all funder and institutional requirements for being considered Open Access.
- Authors cannot use copyrighted material within their article unless that material has also been made available under a similarly liberal license.