Animal Reproduction (AR)
Animal Reproduction (AR)
Thematic Section: 36th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Maternal contributions to pregnancy success: from gamete quality to uterine environment

Anna Carolina Denicol; Luiz Gustavo Bruno Siqueira

Downloads: 1
Views: 136


Abstract: The establishment and maintenance of a pregnancy that goes to term is sine qua non for the long-term sustainability of dairy and beef cattle operations. The oocyte plays a critical role in providing the factors necessary for preimplantation embryonic development. Furthermore, the female, or maternal, environment where oocytes and embryos develop is crucial for the establishment and maintenance of a pregnancy to term. During folliculogenesis, the oocyte must sequentially acquire meiotic and developmental competence, which are the results of a series of molecular events preparing the highly specialized gamete to return to totipotency after fertilization. Given that folliculogenesis is a lengthy process in the cow, the occurrence of disease, metabolic imbalances, heat stress, or other adverse events can make it challenging to maintain oocyte quality. Following fertilization, the newly formed embryo must execute a tightly planned program that includes global DNA remodeling, activation of the embryonic genome, and cell fate decisions to form a blastocyst within a few days and cell divisions. The increasing use of assisted reproductive technologies creates an additional layer of complexity to ensure the highest oocyte and embryo quality given that in vitro systems do not faithfully recreate the physiological maternal environment. In this review, we discuss cellular and molecular factors and events known to be crucial for proper oocyte development and maturation, as well as adverse events that may negatively affect the oocyte; and the importance of the uterine environment, including signaling proteins in the maternal-embryonic interactions that ensure proper embryo development. We also discuss the impact of assisted reproductive technologies in oocyte and embryo quality and developmental potential, and considerations when looking into the prospects for developing systems that allow for in vitro gametogenesis as a tool for assisted reproduction in cattle.


oocyte, embryo, assisted reproduction, developmental competence


Aguiar LH, Hyde KA, Pedroza GH, Denicol AC. Heat stress impairs in vitro development of preantral follicles of cattle. Anim Reprod Sci. 2020;213:106277. PMid:31987328.

Aizawa E, Ozonov EA, Kawamura YK, Dumeau CE, Nagaoka S, Saitou M, Peters AHFM, Wutz A. Comprehensive comparison of female germ cell development in vitro and in vivo identifies epigenetic gene regulation crucial for oocyte development and embryonic competence. bioRxiv. In Press 2023.

Amaral TF, Grazia JGV, Martinhao LAG, De Col F, Siqueira LGB, Viana JHM, Hansen PJ. Actions of CSF2 and DKK1 on bovine embryo development and pregnancy outcomes are affected by composition of embryo culture medium. Sci Rep. 2022;12(1):7503. PMid:35525843.

Anckaert E, Fair T. DNA methylation reprogramming during oogenesis and interference by reproductive technologies: studies in mouse and bovine models. Reprod Fertil Dev. 2015;27(5):739-54. PMid:25976160.

Arat S, Caputcu AT, Cevik M, Akkoc T, Cetinkaya G, Bagis H. Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos. Zygote. 2016;24(4):554-62. PMid:26444069.

Banliat C, Mahé C, Lavigne R, Com E, Pineau C, Labas V, Guyonnet B, Mermillod P, Saint-Dizier M. The proteomic analysis of bovine embryos developed in vivo or in vitro reveals the contribution of the maternal environment to early embryo. BMC Genomics. 2022;23(1):839. PMid:36536309.

Baruselli PS, Ferreira RM, Vieira LM, Souza AH, Bó GA, Rodrigues CA. Use of embryo transfer to alleviate infertility caused by heat stress. Theriogenology. 2020;155:1-11. PMid:32562738.

Behboodi E, Anderson GB, BonDurant RH, Cargill SL, Kreuscher BR, Medrano JF, Murray JD. Birth of large calves that developed from in vitro-derived bovine embryos. Theriogenology. 1995;44(2):227-32. PMid:16727722.

Bertolini M, Mason JB, Beam SW, Carneiro GF, Sween ML, Kominek DJ, Moyer AL, Famula TR, Sainz RD, Anderson GB. Morphology and morphometry of in vivo-and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology. 2002;58(5):973-94. PMid:12212896.

Block J, Bonilla L, Hansen PJ. Efficacy of in vitro embryo transfer in lactating dairy cows using fresh or vitrified embryos produced in a novel embryo culture medium. J Dairy Sci. 2010;93(11):5234-42. PMid:20965338.

Block J, Fischer-Brown AE, Rodina TM, Ealy AD, Hansen PJ. The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation. Theriogenology. 2007;68(2):153-61. PMid:17532038.

Bloise E, Feuer SK, Rinaudo PF. Comparative intrauterine development and placental function of ART concepti: implications for human reproductive medicine and animal breeding. Hum Reprod Update. 2014;20(6):822-39. PMid:24947475.

Blondin P, Bousquet D, Twagiramungu H, Barnes F, Sirard M-A. Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol Reprod. 2002;66(1):38-43. PMid:11751261.

Blondin P, Farin PW, Crosier AE, Alexander JE, Farin CE. In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer. Biol Reprod. 2000;62(2):384-9. PMid:10642577.

Bromfield JJ, Sheldon IM. Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biol Reprod. 2013;88(4):98. PMid:23515670.

Burdge GC, Lillycrop KA. Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr. 2010;30(1):315-39. PMid:20415585.

Calle A, Miranda A, Fernandez-Gonzalez R, Pericuesta E, Laguna R, Gutierrez-Adan A. Male mice produced by in vitro culture have reduced fertility and transmit organomegaly and glucose intolerance to their male offspring. Biol Reprod. 2012;87(2):34. PMid:22649070.

Candelaria JI, Rabaglino MB, Denicol AC. Ovarian preantral follicles are responsive to FSH as early as the primary stage of development. J Endocrinol. 2020;247(2):153-68. PMid:32805705.

Chen Z, Hagen DE, Elsik CG, Ji T, Morris CJ, Moon LE, Rivera RM. Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction. Proc Natl Acad Sci USA. 2015;112(15):4618-23. PMid:25825726.

Chen Z, Robbins KM, Wells KD, Rivera RM. Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith-Wiedemann. Epigenetics. 2013;8(6):591-601. PMid:23751783.

Denicol AC, Block J, Kelley DE, Pohler KG, Dobbs KB, Mortensen CJ, Ortega MS, Hansen PJ. The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo. FASEB J. 2014;28(9):3975-86. PMid:24858280.

Doherty AS, Mann MRW, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000;62(6):1526-35. PMid:10819752.

Ealy AD, Speckhart SL, Wooldridge LK. Cytokines that serve as embryokines in cattle. Animals. 2021;11(8):2313. PMid:34438770.

El Hajj N, Haaf T. Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil Steril. 2013;99(3):632-41. PMid:23357453.

Enright BP, Lonergan P, Dinnyes A, Fair T, Ward FA, Yang X, Boland MP. Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology. 2000;54(5):659-73. PMid:11101029.

Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci USA. 2002;99(5):2890-4. PMid:11867735.

Farin CE, Farmer WT, Farin PW. Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod Fertil Dev. 2010;22(1):75-87. PMid:20003848.

Farin PW, Farin CE. Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development. Biol Reprod. 1995;52(3):676-82. PMid:7756461.

Farin PW, Piedrahita JA, Farin CE. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology. 2006;65(1):178-91. PMid:16266745.

Fernández-Gonzalez R, Moreira P, Bilbao A, Jiménez A, Pérez-Crespo M, Ramírez MA, Fonseca FRD, Pintado B, Gutiérrez-Adán A. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci USA. 2004;101(16):5880-5. PMid:15079084.

Ferraz PA, Burnley C, Karanja J, Viera-Neto A, Santos JEP, Chebel RC, Galvão KN. Factors affecting the success of a large embryo transfer program in Holstein cattle in a commercial herd in the southeast region of the United States. Theriogenology. 2016;86(7):1834-41. PMid:27364084.

Feuer SK, Liu X, Donjacour A, Lin W, Simbulan RK, Giritharan G, Piane LD, Kolahi K, Ameri K, Maltepe E, Rinaudo PF. Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology. 2014;155(5):1956-69. PMid:24684304.

Fields SD, Hansen PJ, Ealy AD. Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology. 2011;75(8):1466-75. PMid:21295834.

Fleming TP, Velazquez MA, Eckert JJ. Embryos, DOHaD and David Barker. J Dev Orig Health Dis. 2015;6(5):377-83. PMid:25952250.

Gardner DK, Harvey AJ. Blastocyst metabolism. Reprod Fertil Dev. 2015;27(4):638-54. PMid:25751298.

Garverick HA, Harris MN, Vogel-Bluel R, Sampson JD, Bader J, Lamberson WR, Spain JN, Lucy MC, Youngquist RS. Concentrations of nonesterified fatty acids and glucose in blood of periparturient dairy cows are indicative of pregnancy success at first insemination. J Dairy Sci. 2013;96(1):181-8. PMid:23141836.

Giritharan G, Talbi S, Donjacour A, Di Sebastiano F, Dobson AT, Rinaudo PF. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction. 2007;134(1):63-72. PMid:17641089.

Goszczynski DE, Cheng H, Demyda-Peyrás S, Medrano JF, Wu J, Ross PJ. In vitro breeding: application of embryonic stem cells to animal production. Biol Reprod. 2019;100(4):885-95. PMid:30551176.

Grazul-Bilska AT, Borowicz PP, Johnson ML, Minten MA, Bilski JJ, Wroblewski R, Redmer DA, Reynolds LP. Placental development during early pregnancy in sheep: vascular growth and expression of angiogenic factors in maternal placenta. Reproduction. 2010;140(1):165-74. PMid:20400519.

Halter S, Reynaud K, Tahir Z, Thoumire S, Chastant-Maillard S, Saint-Dizier M. L’oviducte de mammifère: un organe revisité. Gynécol Obstét Fertil. 2011;39(11):625-9. PMid:22000832.

Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell. 2004;6(1):117-31. PMid:14723852.

Hansen PJ, Dobbs KB, Denicol AC. Programming of the preimplantation embryo by the embryokine colony stimulating factor 2. Anim Reprod Sci. 2014;149(1-2):59-66. PMid:24954585.

Hansen PJ, Tríbulo P. Regulation of present and future development by maternal regulatory signals acting on the embryo during the morula to blastocyst transition - insights from the cow. Biol Reprod. 2019;101(3):526-37. PMid:31220231.

Hasler JF. In-vitro production of cattle embryos: problems with pregnancies and parturition. Hum Reprod. 2000;15(Suppl 5):47-58. PMid:11263537.

Hiendleder S, Wirtz M, Mund C, Klempt M, Reichenbach H-D, Stojkovic M, Weppert M, Wenigerkind H, Elmlinger M, Lyko F, Schmitz OJ, Wolf E. Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses. Biol Reprod. 2006;75(1):17-23. PMid:16554415.

Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M, Hayashi K. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539(7628):299-303. PMid:27750280.

Holm P, Callesen H. In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. Reprod Nutr Dev. 1998;38(6):579-94. PMid:9932292.

Horsthemke B, Ludwig M. Assisted reproduction: the epigenetic perspective. Hum Reprod Update. 2005;11(5):473-82. PMid:15994847.

Inbar-Feigenberg M, Choufani S, Butcher DT, Roifman M, Weksberg R. Basic concepts of epigenetics. Fertil Steril. 2013;99(3):607-15. PMid:23357459.

Kane MT, Morgan PM, Coonan C. Peptide growth factors and preimplantation development. Hum Reprod Update. 1997;3(2):137-57. PMid:9286738.

Kannampuzha-Francis J, Tribulo P, Hansen P. Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on development of the bovine preimplantation embryo. Reprod Fertil Dev. 2017;29(7):1329-39. PMid:27185102.

Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, Gaughan JP, Coutifaris C, Sapienza C. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet. 2009;18(20):3769-78. PMid:19605411.

Kojima Y, Tam OH, Tam PPL. Timing of developmental events in the early mouse embryo. Semin Cell Dev Biol. 2014;34:65-75. PMid:24954643.

Krisher RL, Bavister BD. Responses of oocytes and embryos to the culture environment. Theriogenology. 1998;49(1):103-14. PMid:10732124.

Krisher RL. The effect of oocyte quality on development. J Anim Sci. 2004;82(E-Suppl):E14-23. PMid:15471793.

Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127(19):4195-202. PMid:10976051.

Lafontaine S, Labrecque R, Blondin P, Cue RI, Sirard M-A. Comparison of cattle derived from in vitro fertilization, multiple ovulation embryo transfer, and artificial insemination for milk production and fertility traits. J Dairy Sci. 2023;106(6):4380-96. PMid:37028966.

Latorraca LB, Galvão A, Kelsey B, D’augero J, Rabaglino MB, Fair T. Differential gene expression across bovine oocyte growth phase. Reprod Fertil Dev. 2023;35(2):125-255.

Lazzari G, Wrenzycki C, Herrmann D, Duchi R, Kruip T, Niemann H, Galli C. Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol Reprod. 2002;67(3):767-75. PMid:12193383.

Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction. 2005;130(4):485-95. PMid:16183866.

Leung CY, Zernicka-Goetz M. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and -independent mechanisms. Nat Commun. 2013;4(1):2251. PMid:23903990.

Li Y, Tríbulo P, Bakhtiarizadeh MR, Siqueira LGB, Ji T, Rivera RM, Hansen PJ. Conditions of embryo culture from days 5 to 7 of development alter the DNA methylome of the bovine fetus at day 86 of gestation. J Assist Reprod Genet. 2020;37(2):417-26. PMid:31838628.

Lonergan P, Fair T, Corcoran D, Evans ACO. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology. 2006;65(1):137-52. PMid:16289260.

Lonergan P, Forde N. Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle. Animal. 2014;8(Suppl 1):64-9. PMid:24679216.

Loureiro B, Bonilla L, Block J, Fear JM, Bonilla AQS, Hansen PJ. Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology. 2009;150(11):5046-54. PMid:19797121.

Marei WFA, De Bie J, Xhonneux I, Andries S, Britt JH, Leroy JLMR. Metabolic and antioxidant status during transition is associated with changes in the granulosa cell transcriptome in the preovulatory follicle in high-producing dairy cows at the time of breeding. J Dairy Sci. 2022;105(8):6956-72. PMid:35840405.

Marei WFA, Van den Bosch L, Pintelon I, Mohey-Elsaeed O, Bols PEJ, Leroy JLMR. Mitochondria-targeted therapy rescues development and quality of embryos derived from oocytes matured under oxidative stress conditions: a bovine in vitro model. Hum Reprod. 2019;34(10):1984-98. PMid:31625574.

Market-Velker BA, Fernandes AD, Mann MRW. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol Reprod. 2010;83(6):938-50. PMid:20702853.

Mathew DJ, Peterson KD, Senn LK, Oliver MA, Ealy AD. Ruminant conceptus-maternal interactions: interferon-tau and beyond. J Anim Sci. 2022;100(7):skac123. PMid:35772752.

McEvoy TG, Sinclair KD, Broadbent PJ, Goodhand KL, Robinson JJ. Post-natal growth and development of Simmental calves derived from in vivo or in vitro embryos. Reprod Fertil Dev. 1998;10(6):459-64. PMid:10588375.

McHughes CE, Springer GK, Spate LD, Li R, Woods R, Green MP, Korte SW, Murphy CN, Green JA, Prather RS. Identification and quantification of differentially represented transcripts in in vitro and in vivo derived preimplantation bovine embryos. Mol Reprod Dev. 2009;76(1):48-60. PMid:18449894.

Moorey SE, Hessock EA, Edwards JL. Preovulatory follicle contributions to oocyte competence in cattle: importance of the ever-evolving intrafollicular environment leading up to the luteinizing hormone surge. J Anim Sci. 2022;100(7):skac153. PMid:35772757.

Morton AJ, Candelaria JI, McDonnell SP, Zgodzay DP, Denicol AC. Review: roles of follicle-stimulating hormone in preantral folliculogenesis of domestic animals: what can we learn from model species and where do we go from here? Animal. In Press 2023.

Niemann H, Carnwath JW, Herrmann D, Wieczorek G, Lemme E, Lucas-Hahn A, Olek S. DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell Reprogram. 2010;12(1):33-42. PMid:20132011.

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. 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. 2016;86(4):994-1003. PMid:27125691.

Palma GA, Müller M, Brem G. Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro. J Reprod Fertil. 1997;110(2):347-53. PMid:9306989.

Pan H, O’brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol. 2005;286(2):493-506. PMid:16168984.

Paria BC, Dey SK. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci USA. 1990;87(12):4756-60. PMid:2352946.

Pedroza GH, Lanzon LF, Rabaglino MB, Walker WL, Vahmani P, Denicol AC. Exposure to non-esterified fatty acids in vitro results in changes in the ovarian and follicular environment in cattle. Anim Reprod Sci. 2022;238:106937. PMid:35149437.

Pohler KG, Pereira MHC, Lopes FR, Lawrence JC, Keisler DH, Smith MF, Vasconcelos JLM, Green JA. Circulating concentrations of bovine pregnancy-associated glycoproteins and late embryonic mortality in lactating dairy herds. J Dairy Sci. 2016;99(2):1584-94. PMid:26709163.

Pontes JHF, Nonato-Junior I, Sanches BV, Ereno-Junior JC, Uvo S, Barreiros TRR, Oliveira JA, Hasler JF, Seneda MM. Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology. 2009;71(4):690-7. PMid:18995895.

Rabaglino MB, Salilew-Wondim D, Zolini A, Tesfaye D, Hoelker M, Lonergan P, Hansen PJ. Machine-learning methods applied to integrated transcriptomic data from bovine blastocysts and elongating conceptuses to identify genes predictive of embryonic competence. FASEB J. 2023;37(3):e22809. PMid:36753406.

Ralston A, Rossant J. Genetic regulation of stem cell origins in the mouse embryo. Clin Genet. 2005;68(2):106-12. PMid:15996204.

Ribeiro ES, Gomes G, Greco LF, Cerri RLA, Vieira-Neto A, Monteiro PLJ Jr, Lima FS, Bisinotto RS, Thatcher WW, Santos JEP. Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows. J Dairy Sci. 2016;99(3):2201-20. PMid:26723113.

Rinaudo P, Schultz RM. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction. 2004;128(3):301-11. PMid:15333781.

Rivera RM. Consequences of assisted reproductive techniques on the embryonic epigenome in cattle. Reprod Fertil Dev. 2019;32(2):65-81. PMid:32188559.

Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. 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. 2002;61(2):234-48. PMid:11803560.

Roth Z. Physiology and Endocrinology Symposium: cellular and molecular mechanisms of heat stress related to bovine ovarian function. J Anim Sci. 2015;93(5):2034-44. PMid:26020299.

Salilew-Wondim D, Tesfaye D, Hossain M, Held E, Rings F, Tholen E, Looft C, Cinar U, Schellander K, Hoelker M. Aberrant placenta gene expression pattern in bovine pregnancies established after transfer of cloned or in vitro produced embryos. Physiol Genomics. 2013;45(1):28-46. PMid:23092953.

Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction. 2004;127(6):643-51. PMid:15175501.

Schultz RM, Stein P, Svoboda P. The oocyte-to-embryo transition in mouse: past, present, and future. Biol Reprod. 2018;99(1):160-74. PMid:29462259.

Sinclair KD, McEvoy TG, Maxfield EK, Maltin CA, Young LE, Wilmut I, Broadbent PJ, Robinson JJ. Aberrant fetal growth and development after in vitro culture of sheep zygotes. J Reprod Fertil. 1999;116(1):177-86. PMid:10505068.

Siqueira LG, Silva MVG, Panetto JC, Viana JH. Consequences of assisted reproductive technologies for offspring function in cattle. Reprod Fertil Dev. 2019;32(2):82-97. PMid:32188560.

Siqueira LGB, Dikmen S, Ortega MS, Hansen PJ. Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen. J Dairy Sci. 2017;100(7):5899-908. PMid:28456408.

Siqueira LGB, Torres CAA, Souza ED, Monteiro PLJ Jr, Arashiro EKN, Camargo LSA, Fernandes CAC, Viana JHM. Pregnancy rates and corpus luteum–related factors affecting pregnancy establishment in bovine recipients synchronized for fixed-time embryo transfer. Theriogenology. 2009;72(7):949-58. PMid:19709722.

Sirard MA. Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology. 2001;55(6):1241-54. PMid:11327682.

Sirisathien S, Brackett BG. TUNEL analyses of bovine blastocysts after culture with EGF and IGF-I. Mol Reprod Dev. 2003;65(1):51-6. PMid:12658633.

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. PMid:12654525.

Sternlicht AL, Schultz RM. Biochemical studies of mammalian oogenesis: kinetics of accumulation of total and poly(A)-containing RNA during growth of the mouse oocyte. J Exp Zool. 1981;215(2):191-200. PMid:6168731.

Stewart BM, Block J, Morelli P, Navarette AE, Amstalden M, Bonilla L, Hansen PJ, Bilby TR. Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen. J Dairy Sci. 2011;94(7):3437-45. PMid:21700029.

Thompson JG. Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod Fertil Dev. 1997;9(3):341-54. PMid:9261882.

Tríbulo P, Balzano-Nogueira L, Conesa A, Siqueira LG, Hansen PJ. Changes in the uterine metabolome of the cow during the first 7 days after estrus. Mol Reprod Dev. 2019;86(1):75-87. PMid:30383328.

Tríbulo P, Siqueira LGB, Oliveira LJ, Scheffler T, Hansen PJ. Identification of potential embryokines in the bovine reproductive tract. J Dairy Sci. 2018;101(1):690-704. PMid:29128220.

Urrego R, Rodriguez-Osorio N, Niemann H. Epigenetic disorders and altered gene expression after use of Assisted Reproductive Technologies in domestic cattle. Epigenetics. 2014;9(6):803-15. PMid:24709985.

Valckx SD, Van Hoeck V, Arias-Alvarez M, Maillo V, Lopez-Cardona AP, Gutierrez-Adan A, Berth M, Cortvrindt R, Bols PE, Leroy JL. Elevated non-esterified fatty acid concentrations during in vitro murine follicle growth alter follicular physiology and reduce oocyte developmental competence. Fertil Steril. 2014;102(6):1769-76.E1. PMid:25256931.

van Wagtendonk-de Leeuw AM, Aerts BJ, den Daas JH. Abnormal offspring following in vitro production of bovine preimplantation embryos: a field study. Theriogenology. 1998;49(5):883-94. PMid:10732097.

Vasconcelos JLM, Jardina DTG, Sá OG Fo, Aragon FL, Veras MB. Comparison of progesterone-based protocols with gonadotropin-releasing hormone or estradiol benzoate for timed artificial insemination or embryo transfer in lactating dairy cows. Theriogenology. 2011;75(6):1153-60. PMid:21247621.

Viana J. 2021 statistics of embryo production and transfer in domestic farm animals: a new milestone has been reached: transfers of IVP embryos were over one million worldwide. Embryo Technol Newsl. 2022;40(4):22-40.

Viana JHM. 2017 statistics of embryo production and transfer in domestic farm animals: is it a turning point? In 2017 more in vitro-produced than in vivo-derived embryos were transferred worldwide. Embryo Transf Newsl. 2018;36(4):8-25.

Vigneault C, McGraw S, Massicotte L, Sirard M-A. Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol Reprod. 2004;70(6):1701-9. PMid:14960490.

Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006;7(3):185-99. PMid:16485018.

Wang JX, Norman RJ, Wilcox AJ. Incidence of spontaneous abortion among pregnancies produced by assisted reproductive technology. Hum Reprod. 2004;19(2):272-7. PMid:14747166.

Wang Q, Zhao SX, He JN, Zhao H, Gu BX, Xie JK, Zhao YJ, Zhang CL, Ge ZJ. Repeated superovulation accelerates primordial follicle activation and atresia. Cells. 2022;12(1):92. PMid:36611886.

Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PL, Melo LF, Ochoa JC, Santos JE, Sartori R. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology. 2016;86(1):239-53. PMid:27238438.

Wolf E, Arnold GJ, Bauersachs S, Beier HM, Blum H, Einspanier R, Fröhlich T, Herrler A, Hiendleder S, Kölle S, Prelle K, Reichenbach H-D, Stojkovic M, Wenigerkind H, Sinowatz F. Embryo-maternal communication in bovine - strategies for deciphering a complex cross-talk. Reprod Domest Anim. 2003;38(4):276-89. PMid:12887567.

Wooldridge LK, Keane JA, Rhoads ML, Ealy AD. Bioactive supplements influencing bovine in vitro embryo development. J Anim Sci. 2022;100(7):skac091. PMid:35772761.

Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998;3(3):155-63. PMid:9829550.

Submitted date:

Accepted date:

64f2303ea953951d7f27c0a2 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections