The interaction between the environment and embryo development in assisted reproduction
Urban Besenfelder; Vitezslav Havlicek
Abstract
Keywords
References
Beebe D, Wheeler M, Zeringue H, Walters E, Raty S. Microfluidic technology for assisted reproduction. Theriogenology. 2002;57(1):125-35.
Berglund B. Genetic improvement of dairy cow reproductive performance. Reprod Domest Anim. 2008;43(Suppl 2):89-95.
Besenfelder U, Brem G. Tubal transfer of bovine embryos: a simple endoscopic method reducing long-term exposure of in vitro produced embryos. Theriogenology. 1998;50(5):739-45.
Besenfelder U, Havlicek V, Kuzmany A, Brem G. Endoscopic approaches to manage in vitro and in vivo embryo development: use of the bovine oviduct. Theriogenology. 2010;73(6):768-76.
Besenfelder U, Havlicek V, Moesslacher G, Gilles M, Tesfaye D, Griese J, Hoelker M, Hyttel PM, Laurincik J, Brem G, Schellander K. Endoscopic recovery of early preimplantation bovine embryos: effect of hormonal stimulation, embryo kinetics and repeated collection. Reprod Domest Anim. 2008;43(5):566-72.
Besenfelder U, Havlicek V, Mösslacher G, Brem G. Collection of tubal stage bovine embryos by means of endoscopy. A technique report. Theriogenology. 2001;55(3):837-45.
Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D. Collection, description and transfer of embryos from cattle 10--16 days after oestrus. J Reprod Fertil. 1980;59(1):205-16.
Carter F, Rings F, Mamo S, Holker M, Kuzmany A, Besenfelder U, Havlicek V, Mehta JP, Tesfaye D, Schellander K, Lonergan P. Effect of elevated circulating progesterone concentration on bovine blastocyst development and global transcriptome following endoscopic transfer of in vitro produced embryos to the bovine oviduct. Biol Reprod. 2010;83(5):707-19.
Carvalho AV, Canon E, Jouneau L, Archilla C, Laffont L, Moroldo M, Ruffini S, Corbin E, Mermillod P, Duranthon V. Different co-culture systems have the same impact on bovine embryo transcriptome. Reproduction. 2017;154(5):695-710.
Clark GF. The mammalian zona pellucida: a matrix that mediates both gamete binding and immune recognition? Syst Biol Reprod Med. 2010;56(5):349-64.
Croxatto HB. Physiology of gamete and embryo transport through the fallopian tube. Reprod Biomed Online. 2002;4(2):160-9.
Dickens CJ, Leese HJ. The regulation of rabbit oviduct fluid formation. J Reprod Fertil. 1994;100(2):577-81.
Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim. 2008;43(Suppl 2):260-7.
Dissanayake K, Nõmm M, Lättekivi F, Ord J, Ressaissi Y, Godakumara K, Reshi QUA, Viil J, Jääger K, Velthut-Meikas A, Salumets A, Jaakma Ü, Fazeli A. Oviduct as a sensor of embryo quality: deciphering the extracellular vesicle (EV)-mediated embryo-maternal dialogue. J Mol Med. 2021;99(5):685-97.
Duranthon V, Chavatte-Palmer P. Long term effects of ART: what do animals tell us? Mol Reprod Dev. 2018;85(4):348-68.
Ealy AD, Wooldridge LK, McCoski SR. Board invited review: post-transfer consequences of in vitro-produced embryos in cattle. J Anim Sci. 2019;97(6):2555-68.
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.
Ferraz MAMM, Rho HS, Hemerich D, Henning HHW, van Tol HTA, Hölker M, Besenfelder U, Mokry M, Vos PLAM, Stout TAE, Le Gac S, Gadella BM. An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming. Nat Commun. 2018;9(1):4934.
Ferré LB, Kjelland ME, Strøbech LB, Hyttel P, Mermillod P, Ross PJ. Review: recent advances in bovine
Gad A, Besenfelder U, Rings F, Ghanem N, Salilew-Wondim D, Hossain MM, Tesfaye D, Lonergan P, Becker A, Cinar U, Schellander K, Havlicek V, Hölker M. Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction. Hum Reprod. 2011;26(7):1693-707.
Gad A, Hoelker M, Besenfelder U, Havlicek V, Cinar U, Rings F, Held E, Dufort I, Sirard MA, Schellander K, Tesfaye D. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod. 2012;87(4):100.
Georges M, Charlier C, Hayes B. Harnessing genomic information for livestock improvement. Nat Rev Genet. 2019;20(3):135-56.
Ghersevich S, Massa E, Zumoffen C. Oviductal secretion and gamete interaction. Reproduction. 2015;149(1):R1-14.
González-Brusi L, Algarra B, Moros-Nicolás C, Izquierdo-Rico MJ, Avilés M, Jiménez-Movilla M. A comparative view on the oviductal environment during the periconception period. Biomolecules. 2020;10(12):1690.
Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci USA. 2014;111(11):4139-44.
Havlicek V, Autz A-K, Blaschka C, Hoelker M, Besenfelder U. Collection of embryos and fluid from the bovine oviduct. Anim Reprod. 2022;19(spe 2):e22193.
Havlicek V, Kuzmany A, Cseh S, Brem G, Besenfelder U. The effect of long-term in vivo culture in bovine oviduct and uterus on the development and cryo-tolerance of in vitro produced bovine embryos. Reprod Domest Anim. 2010;45(5):832-7. PMid:19416481.
Hugentobler S, Morris DG, Kane MT, Sreenan JM. In situ oviduct and uterine pH in cattle. Theriogenology. 2004;61(7-8):1419-27.
Hugentobler SA, Diskin MG, Leese HJ, Humpherson PG, Watson T, Sreenan JM, Morris DG. Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol Reprod Dev. 2007a;74(4):445-54.
Hugentobler SA, Humpherson PG, Leese HJ, Sreenan JM, Morris DG. Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Mol Reprod Dev. 2008;75(3):496-503.
Hugentobler SA, Morris DG, Sreenan JM, Diskin MG. Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine. Theriogenology. 2007b;68(4):538-48.
Hugentobler SA, Sreenan JM, Humpherson PG, Leese HJ, Diskin MG, Morris DG. Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood. Reprod Fertil Dev. 2010;22(4):684-94.
Hunter RH. Components of oviduct physiology in eutherian mammals. Biol Rev Camb Philos Soc. 2012;87(1):244-55.
Hunter RH. Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol Reprod Dev. 2008;75(1):167-74.
Jordaens L, Van Hoeck V, De Bie J, Berth M, Marei WFA, Desmet KLJ, Bols PEJ, Leroy JLMR. Non-esterified fatty acids in early luteal bovine oviduct fluid mirror plasma concentrations: an ex vivo approach. Reprod Biol. 2017;17(3):281-4.
Kavanaugh JF, Grippo AA, Killian GJ. Cannulation of the bovine ampullary and isthmic oviduct. J Invest Surg. 1992;5(1):11-7.
Kavanaugh JF, Killian GJ. Bovine oviductal cannulations. J Invest Surg. 1988;1(3):201-8.
Killian GJ, Chapman DA, Kavanaugh JF, Deaver DR, Wiggin HB. Changes in phospholipids, cholesterol and protein content of oviduct fluid of cows during the oestrous cycle. J Reprod Fertil. 1989;86(2):419-26.
Kölle S, Reese S, Kummer W. New aspects of gamete transport, fertilization, and embryonic development in the oviduct gained by means of live cell imaging. Theriogenology. 2010;73(6):786-95.
Lazzari G, Colleoni S, Lagutina I, Crotti G, Turini P, Tessaro I, Brunetti D, Duchi R, Galli C. Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology. 2010;73(6):748-57.
Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121(3):339-46.
Leese HJ. The formation and function of oviduct fluid. J Reprod Fertil. 1988;82(2):843-56.
Lonergan P, Fair T. In vitro-produced bovine embryos: dealing with the warts. Theriogenology. 2008;69(1):17-22.
Lonergan P, Rizos D, Kanka J, Nemcova L, Mbaye AM, Kingston M, Wade M, Duffy P, Boland MP. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction. 2003;126(3):337-46.
Lonergan P, Sánchez JM. Symposium review: progesterone effects on early embryo development in cattle. J Dairy Sci. 2020;103(9):8698-707.
Lonergan P. State-of-the-art embryo technologies in cattle. Soc Reprod Fertil Suppl. 2007;64:315-25. PMid:17491156.
Lopera-Vasquez R, Hamdi M, Maillo V, Lloreda V, Coy P, Gutierrez-Adan A, Bermejo-Alvarez P, Rizos D. Effect of bovine oviductal fluid on development and quality of bovine embryos produced in vitro. Reprod Fertil Dev. 2017;29(3):621-9.
Lucy MC. Reproductive loss in high-producing dairy cattle: where will it end? J Dairy Sci. 2001;84(6):1277-93.
Maillo V, Rizos D, Besenfelder U, Havlicek V, Kelly AK, Garrett M, Lonergan P. Influence of lactation on metabolic characteristics and embryo development in postpartum Holstein dairy cows. J Dairy Sci. 2012;95(7):3865-76.
May-Panloup P, Vignon X, Chrétien MF, Heyman Y, Tamassia M, Malthièry Y, Reynier P. Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod Biol Endocrinol. 2005;3(1):65.
Menezo Y, Guerin P. The mammalian oviduct: biochemistry and physiology. Eur J Obstet Gynecol Reprod Biol. 1997;73(1):99-104.
Mertens E, Besenfelder U, Gilles M, Hölker M, Rings F, Havlicek V, Schellander K, Herrler A. Influence of in vitro culture of bovine embryos on the structure of the zona pellucida. Reprod Fertil Dev. 2007;19(1):211-2.
Mertens E, Gilles M, Rings F, Hoelker M, Schellander K, Herrler A. Influence of in vitro culture of bovine embryos on the structure of the zona pellucida. Reprod Domes Anim. 2006;41(Suppl 1):23.
Merton JS, Roos AP, Mullaart E, Ruigh L, Kaal L, Vos PL, Dieleman SJ. Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology. 2003;59(2):651-74.
Negrón-Pérez VM, Hansen PJ. The bovine embryo hatches from the zona pellucida through either the embryonic or abembryonic pole. J Assist Reprod Genet. 2017;34(6):725-31.
Neira JA, Tainturier D, Peña 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.
Neubrand L, Pothmann H, Besenfelder U, Havlicek V, Aurich C, Gabler C, Drillich M, Wagener K. In vivo dynamics of oviduct-specific glycoprotein 1 (OVGP1) in dairy cows and heifers. Reprod Domest Anim. 2022;57(Suppl 1):35.
Neubrand L, Pothmann H, Havlicek V, Besenfelder U, Aurich C, Drillich M, Gabler C, Wagener K. Oestrous cycle dependent alterations in the mRNA abundance of pro-inflammatory factors in the bovine oviductal epithelium in vivo. Reprod Domest Anim. 2021;56(Suppl 1):45.
Papp SM, Fröhlich T, Radefeld K, Havlicek V, Kösters M, Yu H, Mayrhofer C, Brem G, Arnold GJ, Besenfelder U. A novel approach to study the bovine oviductal fluid proteome using transvaginal endoscopy. Theriogenology. 2019;132:53-61.
Pothmann H, Havlicek V, Besenfelder U, Drillich M. Different methods for in situ collection of samples from the bovine oviduct. Reprod Domest Anim. 2017;52(Suppl 3):124-5.
Pothmann H, Ibrahim M, Besenfelder U, Havlicek V, Drillich M, Gabler C. Hyperketonemia affects mRNA expression of selected pro-inflammatory factors and metabolic enzymes in the endometrium and oviduct of postpartum dairy cows. Reprod Domest Anim. 2022;57(Suppl 3):18.
Radefeld K, Papp S, Havlicek V, Morrell JM, Brem G, Besenfelder U. Endoscopy-mediated intratubal insemination in the cow - development of a novel minimally invasive AI technique. Theriogenology. 2018;115:117-23.
Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293(5532):1089-93.
Rizos D, Carter F, Besenfelder U, Havlicek V, Lonergan P. Contribution of the female reproductive tract to low fertility in postpartum lactating dairy cows. J Dairy Sci. 2010a;93(3):1022-9.
Rizos D, Ramirez MA, Pintado B, Lonergan P, Gutierrez-Adan A. Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct. Theriogenology. 2010b;73(6):777-85.
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.
Roberts GP, Parker JM, Symonds HW. Proteins in the luminal fluid from the bovine oviduct. J Reprod Fertil. 1975;45(2):301-13.
Rodríguez-Alonso B, Hamdi M, Sánchez JM, Maillo V, Gutierrez-Adan A, Lonergan P, Rizos D. An approach to study the local embryo effect on gene expression in the bovine oviduct epithelium in vivo. Reprod Domest Anim. 2019;54(12):1516-23.
Rodríguez-Alonso B, Sánchez JM, Hamdi M, McDonald M, Havlicek V, Besenfelder U, Lonergan P, Rizos D. Asynchrony between the early embryo and the reproductive tract affects subsequent embryo development in cattle. Reprod Fertil Dev. 2020;32(6):564-71.
Rowson LE, Moor RM, Lawson RA. Fertility following egg transfer in the cow; effect of method, medium and synchronization of oestrus. J Reprod Fertil. 1969;18(3):517-23.
Roxström A, Strandberg E, Berglund B, Emanuelson U, Philipsson J. Genetic and environmental correlations among female fertility traits and milk production indifferent parities of Swedish red and white dairy cattle. Acta Agric Scand A Anim Sci. 2001;51(1):7-14.
Ruckebusch Y, Bayard F. Motility of the oviduct and uterus of the cow during the oestrous cycle. J Reprod Fertil. 1975;43(1):23-32.
Saint-Dizier M, Schoen J, Chen S, Banliat C, Mermillod P. Composing the early embryonic microenvironment: physiology and regulation of oviductal secretions. Int J Mol Sci. 2020;21(1):223.
Salilew-Wondim D, Gebremedhn S, Hoelker M, Tholen E, Hailay T, Tesfaye D. The role of MicroRNAs in mammalian fertility: from gametogenesis to embryo implantation. Int J Mol Sci. 2020;21(2):585.
Salilew-Wondim D, Saeed-Zidane M, Hoelker M, Gebremedhn S, Poirier M, Pandey HO, Tholen E, Neuhoff C, Held E, Besenfelder U, Havlicek V, Rings F, Fournier E, Gagné D, Sirard MA, Robert C, Gad A, Schellander K, Tesfaye D. Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation. BMC Genomics. 2018;19(1):424.
Sirard M-Á. How the environment affects early embryonic development. Reprod Fertil Dev. 2021;34(2):203-13. PMid:35231267.
Sirard M-A. The influence of in vitro fertilization and embryo culture on the embryo epigenetic constituents and the possible consequences in the bovine model. J Dev Orig Health Dis. 2017;8(4):411-7.
Stroud B. The year 2009 worldwide statistics of embryo transfer in domestic farm animals. Champaign: IETS; 2010. IETS Statistics and Data Retrieval Committee Report. IETS Data Retrieval Committee. Embryo Technology Newsletter.
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.
Tšuiko O, Catteeuw M, Esteki MZ, Destouni A, Pascottini OB, Besenfelder U, Havlicek V, Smits K, Kurg A, Salumets A, D’Hooghe T, Voet T, Van Soom A, Vermeesch JR. Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos. Hum Reprod. 2017;32(11):2348-57. PMid:29040498.
Uhrín V. Microscopic structure of the epithelium of the oviducts in cows during the estrus cycle. Vet Med. 1983;28(3):145-56. In Slovak. PMid:6405533.
Van der Valk J, Bieback K, Buta C, Cochrane B, Dirks WG, Fu J, Hickman JJ, Hohensee C, Kolar R, Liebsch M, Pistollato F, Schulz M, Thieme D, Weber T, Wiest J, Winkler S, Gstraunthaler G. Fetal Bovine Serum (FBS): past - present - future. ALTEX. 2018;35(1):99-118.
Van der Valk J, Brunner D, Smet KD, Svenningsen AF, Honegger P, Knudsen LE, Lindl T, Noraberg J, Price A, Scarino ML, Gstraunthaler G. Optimization of chemically defined cell culture media--replacing fetal bovine serum in mammalian in vitro methods. Toxicol In Vitro. 2010;24(4):1053-63.
Van der Weijden VA, Chen S, Bauersachs S, Ulbrich SE, Schoen J. Gene expression of bovine embryos developing at the air-liquid interface on oviductal epithelial cells (ALI-BOEC). Reprod Biol Endocrinol. 2017;15(1):91.
Van Soom A, Wrathall AE, Herrler A, Nauwynck HJ. Is the zona pellucida an efficient barrier to viral infection? Reprod Fertil Dev. 2010;22(1):21-31.
Viana JHM. 2019 statistics of embryo production and transfer in domestic farm animals. Embryo industry on a new level: over one million embryos produced in vitro. Embryo Technol Newsl. 2019;36(4):1-15.
Viana JHM. 2021 statistics of embryo production and transfer in domestic farm animals. World embryo industry grows despite the pandemic. Embryo Technol Newsl. 2021;39(4):22-40.
Viuff D, Palsgaard A, Rickords L, Lawson LG, Greve T, Schmidt M, Avery B, Hyttel P, Thomsen PD. Bovine embryos contain a higher proportion of polyploid cells in the trophectoderm than in the embryonic disc. Mol Reprod Dev. 2002;62(4):483-8.
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.
Yániz JL, Lopez-Gatius F, Santolaria P, Mullins KJ. Study of the functional anatomy of bovine oviductal mucosa. Anat Rec. 2000;260(3):268-78.
Submitted date:
03/08/2023
Accepted date:
06/28/2023