Well-of-the-well (WOW) versus polyester mesh (PM): a comparison of single-embryo culture systems in bovines

Authors

  • Daniel Contreras-Benicio Autonomous University of Chihuahua
  • Beatriz Elena Castro-Valenzuela Autonomous University of Chihuahua
  • Juan Alberto Grado-Ahuir Autonomous University of Chihuahua
  • María Eduviges Burrola-Barraza Autonomous University of Chihuahua

DOI:

https://doi.org/10.17533/udea.rccp.v35n2a03

Keywords:

bovine embryo, embryo quality, embryo recovery, in vitro culture, in vitro embryo production, polyester mesh culture, single-embryo culture, well-of-the-well culture

Abstract


Background: Mexico is innovating in the livestock industry through in vitro generation of bovine embryos with technologies such as well-of-the-well (WOW) and polyester mesh (PM) single-embryo culture systems. These techniques allow to maintain embryos in separate areas of a shared culture medium. Objective: To compare the quantity and quality of bovine embryos produced in WOW and PM culture systems versus the conventional (CG) culture system. Methods: In total, 345 embryos fertilized in vitro were evaluated for blastocyst yield in the three culture systems. To count blastocyst cell numbers, 69 embryos in each system were differentially stained for trophectoderm (TE), inner cell mass (ICM), and apoptotic cells. A qPCR gene expression analysis was performed for embryos in all three systems. Results: The WOW, PM and CG systems developed similar amount of blastocysts (41, 35 and 36%, respectively; p>0.05). Blastocysts in all three systems showed adequate amounts of ICM and apoptotic cells. Blastocysts in the PM system showed a greater number of TE cells [63.7 versus 58.6% in the CG system (p<0.05)]. Relative mRNA expression of the embryonic genes POUF5F1, GNAS and TP53 did not differ significantly among systems (p>0.05). The ATP5B expression was higher in WOW than in PM (p<0.05), but similar to CG (p>0.05). The TJP3 expression was higher in PM than in WOW and CG (p<0.05). Expression of ID2 and CLDN4 was higher in WOW than in PM and CG (p<0.05). The biplot graphic from Principal Component Analysis (PCA) revealed that CG was located near degenerated embryos, whereas PM was located near arrested embryos, larger ICM and TE, and TJP3 expression. The WOW was located toward blastocysts, morulae, and expression of CLDN4, ID2 and GNAS. Conclusion: Compared with CG, both the PM and WOW systems are good options for culturing single embryos in the bovine model. Moreover, the PCA results suggest that embryos developed in the WOW system have greater capacity for generating blastocysts with increased ability to form TE and ICM layers, which might improve implantation.

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Author Biographies

Daniel Contreras-Benicio, Autonomous University of Chihuahua

https://orcid.org/0000-0002-7191-9095
Faculty of Zootechnics and Ecology, Autonomous University of Chihuahua, Chihuahua, Mexico.

Beatriz Elena Castro-Valenzuela, Autonomous University of Chihuahua

https://orcid.org/0000-0003-1703-9537
Faculty of Zootechnics and Ecology, Autonomous University of Chihuahua, Chihuahua, Mexico.

Juan Alberto Grado-Ahuir, Autonomous University of Chihuahua

https://orcid.org/0000-0003-0040-6134
Faculty of Zootechnics and Ecology, Autonomous University of Chihuahua, Chihuahua, Mexico.

María Eduviges Burrola-Barraza, Autonomous University of Chihuahua

https://orcid.org/0000-0002-6945-4604
Faculty of Zootechnics and Ecology, Autonomous University of Chihuahua, Chihuahua, Mexico.

References

Adjaye J, Herwig R, Brink TC, Herrmann D, Greber B, Sudheer S, Groth D, Carnwath JW, Lehrach H, Niemann H. Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Physiol Genomics 2007; 31(2):315-327. DOI: http://doi.org/10.1152/physiolgenomics.00041.2007

Betts D, King W. Genetic regulation of embryo death and senescence. Theriogenology 2001; 55(1):171-191. DOI: https://doi.org/10.1016/S0093-691X(00)00453-2

Bougarn S, Cunha P, Gilbert FB, Meurens F, Rainard P. Technical note: Validation of candidate reference genes for normalization of quantitative PCR in bovine mammary epithelial cells responding to inflammatory stimuli. J Dairy Sci 2011; 94(5):2425-2430. DOI: http://doi.org/10.3168/jds.2010-3859

Byrne A, Southgate J, Brison D, Leese H. Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. Repro 1999; 117(1):97-105. DOI: https://doi.org/10.1530/jrf.0.1170097

Corcoran D, Fair T, Park S, Rizos D, Patel OV, Smith GW, Coussens PM, Ireland JJ, Boland MP, Evans AC, Lonergan P. Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Repro 2006; 131(4):651-660. DOI: http://doi.org/10.1530/rep.1.01015

Dai SJ, Xu CL, Wang J, Sun YP, Chian RC. Effect of culture medium volume and embryo density on early mouse embryonic development: tracking the development of the individual embryo. J Assist Reprod Genet 2012; 29(7):617-623. DOI: http://doi.org/10.1007/s10815-012-9744-8

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):2555-2568. DOI: http://doi.org/10.1093/jas/skz116

El-Aziz AHA, Mahrous UE, Kamel SZ, Sabed AA. Factors Influencing in vitro Production of Bovine Embryos: A Review. Asian J Anim Vet Adv 2016; 11(12):737-756. DOI: http://doi.org/10.3923/ajava.2016.737.756

Fleming TP, Sheth B, Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci 2001; 6(6):D1000-1007.

Fouladi-Nashta A, Alberio R, Kafi M, Nicholas B, Campbell K, Webb R. Differential staining combined with TUNEL labelling to detect apoptosis in preimplantation bovine embryos. Reprod Biomed Online 2005; 10(4):497-502. DOI: https://doi.org/10.1016/S1472-6483(10)60827-9

Fujita T, Umeki H, Shimura H, Kugumiya K, Shiga K. Effect of group culture and embryo-culture conditioned medium on development of bovine embryos. J Reprod Dev 2006; 52(1):137-142. DOI: https://doi.org/10.1262/jrd.16084

Furuse M, Moriwaki K. The role of claudin-based tight junctions in morphogenesis. Ann N Y Acad Sci 2009; 1165(58-61. DOI: http://doi.org/10.1111/j.1749-6632.2009.04441.x

Gad A, Schellander K, Hoelker M, Tesfaye D. Transcriptome profile of early mammalian embryos in response to culture environment. Anim Reprod Sci 2012; 134(1-2):76-83. DOI: http://doi.org/10.1016/j.anireprosci.2012.08.014

Garcia EV, Hamdi M, Barrera AD, Sanchez-Calabuig MJ, Gutierrez-Adan A, Rizos D. Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Repro 2017; 153(5):631-643. DOI: http://doi.org/10.1530/REP-16-0654

González-Mariscal L, Quirós M, Diaz-Coranguez M. ZO proteins and redox-dependent processes. Antioxidants & redox signaling 2011; 15(5):1235-1253. DOI: http://doi.org/10.1089/ars.2011.3913

Goovaerts IG, Leroy JL, Jorssen EP, Bols PE. Noninvasive bovine oocyte quality assessment: possibilities of a single oocyte culture. Theriogenology 2010; 74(9):1509-1520. DOI: http://doi.org/10.1016/j.theriogenology.2010.06.022

Gopichandran N, Leese HJ. The effect of paracrine/autocrine interactions on the in vitro culture of bovine preimplantation embryos. Repro 2006; 131(2):269-277. DOI: http://doi.org/10.1530/rep.1.00677

GuimarÃes ASB, Rocha LF, Jesus RDLd, Vasconcelos GL, Anghinoni G, Santana ALA, Barbosa LP. In vitro performance of Zebu (Bos indicus) and Taurus (Bos taurus) donor cow embryos. Rev bras saúde prod anim 2020; 21(1):1-11. DOI: http://doi.org/10.1590/s1519-994021200142020

Guo G, Huss M, Tong GQ, Wang C, Sun LL, Clarke ND, Robson P. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 2010; 18(4):675-685. DOI: https://doi.org/10.1016/j.devcel.2010.02.012

Hansen PJ. Implications of Assisted Reproductive Technologies for Pregnancy Outcomes in Mammals. Annu Rev Anim Biosci 2020a; 8(395-413. DOI: http://doi.org/10.1146/annurev-animal-021419-084010

Hansen PJ. The incompletely fulfilled promise of embryo transfer in cattle-why aren't pregnancy rates greater and what can we do about it? J Anim Sci 2020b; 98(11): DOI: http://doi.org/10.1093/jas/skaa288

Jiang Z, Dong H, Zheng X, Marjani SL, Donovan DM, Chen J, Tian XC. mRNA levels of imprinted genes in bovine in vivo oocytes, embryos and cross species comparisons with humans, mice and pigs. Sci Rep 2015; 5(1):1-10. DOI: http://doi.org/10.1038/srep17898

Khatib H. Imprinting of Nesp55 gene in cattle. Mamm Genome 2004; 15(8):663-667. DOI: http://doi.org//10.1007/s00335-004-2331-2

Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update 2001; 7(4):419-427. DOI: https://doi.org/10.1093/humupd/7.4.419

Kiener TK, Sleptsova-Friedrich I, Hunziker W. Identification, tissue distribution and developmental expression of tjp1/zo-1, tjp2/zo-2 and tjp3/zo-3 in the zebrafish, Danio rerio. Gene Expr Patterns 2007; 7(7):767-776. DOI: http://doi.org/10.1016/j.modgep.2007.05.006

Kirchhof N, Carnwath J, Lemme E, Anastassiadis K, Scholer H, Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 2000; 63(6):1698-1705. DOI: https://doi.org/10.1095/biolreprod63.6.1698

Komori K, Fujii S, Montagne K, Nakamura H, Kimura H, Otake K, Fujii T, Sakai Y. Development of a well-of-the-well system-based embryo culture plate with an oxygen sensing photoluminescent probe. Sens Actuators B Chem 2012; 162(1):278-283. DOI: http://doi.org/10.1016/j.snb.2011.12.078

Kues W, Sudheer S, Herrmann D, Carnwath J, Havlicek V, Besenfelder U, Lehrach H, Adjaye J, Niemann H. Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc Natl Acad Sci USA 2008; 105(50):19768-19773. DOI: https://doi.org/10.1073/pnas.0805616105

Liang M, Ayanga B, Du S, Godwin AK, Hartsock JK, Evans SC. Ovca1, a candidate gene of the genetic modifier of Tp53, Mop2, affects mouse embryonic lethality. Genes Chromosom Cancer 2008; 47(4):315-325. DOI: https://doi.org/10.1002/gcc.20535

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25(4):402-408. DOI: http://doi.org/10.1006/meth.2001.1262

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):621-629. DOI: http://doi.org/10.1071/RD15238

Lopes JS, Alcazar-Trivino E, Soriano-Ubeda C, Hamdi M, Canovas S, Rizos D, Coy P. Reproductive Outcomes and Endocrine Profile in Artificially Inseminated versus Embryo Transferred Cows. Animals 2020; 10(8):DOI: http://doi.org/10.3390/ani10081359

Lopez-Damian EP, Jimenez-Medina JA, Alarcon MA, Lammoglia MA, Hernandez A, Galina CS, Fiordelisio T. Cryopreservation induces higher oxidative stress levels in Bos indicus embryos compared with Bos taurus. Theriogenology 2020; 143(74-81. DOI: http://doi.org/10.1016/j.theriogenology.2019.12.001

Marianowski P, Szymusik I, Grzechocinska B, Cyganek A. The comparison of two different embryo culture methods in the course of in vitro fertilization program. Folia Histochem Cytobiol 2007; 45(I):115-117.

Maylem ERS, Leoveras MED, Atabay EC, Atabay EP. Assessing the Quality of Bovine Embryos Produced In Vitro Through the Inner Cell Mass and Trophectoderm Ratio. Philipp J Sci 2017; 146(4):469-474.

Meo SC, Yamazaki W, Ferreira CR, Perecin F, Saraiva NZ, Leal CL, Garcia JM. Parthenogenetic activation of bovine oocytes using single and combined strontium, ionomycin and 6-dimethylaminopurine treatments. Zygote 2007; 15(4):295-306. DOI: http://doi.org/10.1017/S0967199407004285

Monteiro F, Freitas E, Melo D, Carvalho L, Teixeira A, Coelho L, Trinca L, Barros C. Resistance of embryos from Bos indicus cattle during early stages of in vitro development to heat shock compared to embryos crossbred from crossbred cattle. Anim Reprod 2018; 4(1):51-58.

Moriwaki K, Tsukita S, Furuse M. Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos. Dev Biol 2007; 312(2):509-522. DOI: https://doi.org/10.1016/j.ydbio.2007.09.049

Paria B, Dey S. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci USA 1990; 87(12):4756-4760. DOI: https://doi.org/10.1073/pnas.87.12.4756

Paula-Lopes F, Lima RSd, Satrapa RA, Barros CM. Physiology and endocrinology symposium: influence of cattle genotype (Bos indicus vs. Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature. J Anim Scie 2013; 91(3):1143-1153. DOI: https://doi.org/10.2527/jas.2012-5802

Piedrahita JA. The role of imprinted genes in fetal growth abnormalities. Birth Defects Res A Clin Mol Teratol 2011; 91(8):682-692. DOI: https://doi.org/10.1002/bdra.20795

Roberts RM, Ezashi T, Das P. Trophoblast gene expression: transcription factors in the specification of early trophoblast. Reprod Biol Endocrinol 2004; 2(1):1-9. DOI: http://doi.org/10.1186/1477-7827-2-47

Roth Z. Stress‐induced alterations in oocyte transcripts are further expressed in the developing blastocyst. Mol Reprod Dev 2018; 85(11):821-835. DOI: https://doi.org/10.1002/mrd.23045

Ruddock NT, Wilson KJ, Cooney MA, Korfiatis NA, Tecirlioglu RT, French AJ. Analysis of imprinted messenger RNA expression during bovine preimplantation development. Biol Reprod 2004; 70(4):1131-1135. DOI: https://doi.org/10.1095/biolreprod.103.022236

Salvador I, Cebrian Serrano A, Salamone DF, Silvestre M. Effect of number of oocytes and embryos on in vitro oocyte maturation, fertilization and embryo development in bovine. Span J Agric Res 2011; 9(3):744-752.

Scanavez A, Campos C, Santos R. Pregnancy and pregnancy loss rates in recipients of bovine embryos produced in vitro. Arq Bras Med Vet Zootec 2013; 65(3):722-728. DOI: https://doi.org/10.1590/S0102-09352013000300017

Schiffmacher AT, Keefer CL. CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT‐1 cells. Mol Reprod Dev 2013; 80(10):826-839. DOI: https://doi.org/10.1002/mrd.22212

Serafini PC, Silva ID, Smith GD, Motta EL, Rocha AM, Baracat EC. Endometrial claudin-4 and leukemia inhibitory factor are associated with assisted reproduction outcome. Reprod Biol Endocrinol 2009; 7(1):1-9. DOI: http://doi.org/10.1186/1477-7827-7-30

Sikora KM, Magee DA, Berkowicz EW, Berry DP, Howard DJ, Mullen MP, Evans RD, MacHugh DE, Spillane C. DNA sequence polymorphisms within the bovine guanine nucleotide-binding protein Gs subunit alpha (Gsα)-encoding (GNAS) genomic imprinting domain are associated with performance traits. BMC Genet 2011; 12(1):4.

Somfai T, Inaba Y, Aikawa Y, Ohtake M, Kobayashi S, Akai T, Hattori H, Konishi K, Imai K. Culture of bovine embryos in polyester mesh sections: the effect of pore size and oxygen tension on in vitro development. Reprod Domest Anim 2010; 45(6):1104-1109. DOI: http://doi.org/10.1111/j.1439-0531.2009.01502.x

Sugimura S, Akai T, Hashiyada Y, Somfai T, Inaba Y, Hirayama M, Yamanouchi T, Matsuda H, Kobayashi S, Aikawa Y, Ohtake M, Kobayashi E, Konishi K, Imai K. Promising system for selecting healthy in vitro-fertilized embryos in cattle. PLoS One 2012; 7(5):e36627. DOI: http://doi.org/10.1371/journal.pone.0036627

Sugimura S, Akai T, Somfai T, Hirayama M, Aikawa Y, Ohtake M, Hattori H, Kobayashi S, Hashiyada Y, Konishi K, Imai K. Time-lapse cinematography-compatible polystyrene-based microwell culture system: a novel tool for tracking the development of individual bovine embryos. Biol Reprod 2010; 83(6):970-978. DOI: http://doi.org/10.1095/biolreprod.110.085522

Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod Biomed Online 2001; 3(1):25-29.

DOI: http://doi.org/10.1016/s1472-6483(10)61960-8

Thurston A, Taylor J, Gardner J, Sinclair KD, Young LE. Monoallelic expression of nine imprinted genes in the sheep embryo occurs after the blastocyst stage. Repro 2008; 135(1):29. DOI: http://doi.org/10.1530/REP-07-0211

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):803-815. DOI: http://doi.org/10.4161/epi.28711

Vajta G, Korösi T, Du Y, Nakata K, Ieda S, Kuwayama M, Nagy ZP. The Well-of-the-Well system: an efficient approach to improve embryo development. Reprod Biomed Online 2008; 17(1):73-81. DOI: https://doi.org/10.1016/S1472-6483(10)60296-9

Vajta G, Peura T, Holm P, Paldi A, Greve T, Trounson A, Callesen H. New method for culture of zona‐included or zona‐free embryos: The Well of the Well (WOW) system. Mol Reprod Dev 2000; 55(3):256-264.

Vajta G, Rienzi L, Bavister BD. Zona-free embryo culture: is it a viable option to improve pregnancy rates? Reprod Biomed Online 2010a; 21(1):17-25. DOI: https://doi.org/10.1016/j.rbmo.2010.03.014

Vajta G, Rienzi L, Cobo A, Yovich J. Embryo culture: can we perform better than nature? Reprod Biomed Online 2010b; 20(4):453-469. DOI: https://doi.org/10.1016/j.rbmo.2009.12.018

Van Eijk M, Van Rooijen M, Modina S, Scesi L, Folkers G, Van Tol H, Bevers M, Fisher S, Lewin H, Rakacolli D. Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol Reprod 1999; 60(5):1093-1103. DOI: https://doi.org/10.1095/biolreprod60.5.1093

Xie Y, Awonuga A, Liu J, Rings E, Puscheck EE, Rappolee DA. Stress induces AMPK-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells [corrected]. Stem Cells Dev 2013; 22(10):1564-1575. DOI: https://doi.org/10.1089/scd.2012.0352

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2022-04-05

How to Cite

Contreras-Benicio, D., Castro-Valenzuela, B. E., Grado-Ahuir, J. A., & Burrola-Barraza, M. E. (2022). Well-of-the-well (WOW) versus polyester mesh (PM): a comparison of single-embryo culture systems in bovines. Revista Colombiana De Ciencias Pecuarias, 35(2), 93–108. https://doi.org/10.17533/udea.rccp.v35n2a03

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