Understanding conceptus–maternal interactions: what tools do we need to develop?
Zenab Butt A , Haidee Tinning A , Mary J O’Connell B , Jonathan Fenn B , Ramiro Alberio C and Niamh Forde A *A
B
C
Abstract
Communication between the maternal endometrium and developing embryo/conceptus is critical to support successful pregnancy to term. Studying the peri-implantation period of pregnancy is critical as this is when most pregnancy loss occurs in cattle. Our current understanding of these interactions is limited, due to the lack of appropriate in vitro models to assess these interactions. The endometrium is a complex and heterogeneous tissue that is regulated in a transcriptional and translational manner throughout the oestrous cycle. While there are in vitro models to study endometrial function, they are static and 2D in nature or explant models and are limited in how well they recapitulate the in vivo endometrium. Recent developments in organoid systems, microfluidic approaches, extracellular matrix biology, and in silico approaches provide a new opportunity to develop in vitro systems that better model the in vivo scenario. This will allow us to investigate in a more high-throughput manner the fundamental molecular interactions that are required for successful pregnancy in cattle.
Keywords: endometrium, gene expression, in vitro models, in silico models, interferon tau, pregnancy, progesterone, uterus.
References
Adhikari B, Lee CN, Khadka VS, et al. (2022) RNA-Sequencing based analysis of bovine endometrium during the maternal recognition of pregnancy. BMC Genomics 23, 494.
| Crossref | Google Scholar | PubMed |
Ahn J, Yoon MJ, Hong SH, et al. (2021) Three-dimensional microengineered vascularised endometrium-on-a-chip. Human Reproduction 36(10), 2720-2731.
| Crossref | Google Scholar | PubMed |
Akbulut A, Ertugrul E, Topcu V (2018) Fetal health status prediction based on maternal clinical history using machine learning techniques. Computer Methods and Programs in Biomedicine 163, 87-100.
| Crossref | Google Scholar | PubMed |
Araya J, Rodriguez A, Lagos-SanMartin K, et al. (2021) Maternal thyroid profile in first and second trimester of pregnancy is correlated with gestational diabetes mellitus through machine learning. Placenta 103, 82-85.
| Crossref | Google Scholar | PubMed |
Ault-Seay TB, Payton RR, Moorey SE, et al. (2022) Endometrial gene expression in response to lipopolysaccharide between estrous cycle phases and uterine horns in cattle. Frontiers in Animal Science 3, 939876.
| Crossref | Google Scholar |
Awad M, Kizaki K, Ishiguro-Oonuma T, et al. (2020) Secreted protein of Ly6 domain 1 enhanced bovine trophoblastic cell migration activity. In Vitro Cellular & Developmental Biology – Animal 56(10), 827-831.
| Crossref | Google Scholar | PubMed |
Bedzhov I, Zernicka-Goetz M (2014) Self-organizing properties of mouse pluripotent cells initiate morphogenesis upon implantation. Cell 156(5), 1032-1044.
| Crossref | Google Scholar | PubMed |
Bentwich I, Avniel A, Karov Y, et al. (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nature Genetics 37(7), 766-770.
| Crossref | Google Scholar | PubMed |
Borges ÁM, Healey GD, Sheldon IM (2012) Explants of intact endometrium to model bovine innate immunity and inflammation ex vivo. American Journal of Reproductive Immunology 67(6), 526-539.
| Crossref | Google Scholar | PubMed |
Brooks K, Burns G, Spencer TE (2014) Conceptus elongation in ruminants: roles of progesterone, prostaglandin, interferon tau and cortisol. Journal of Animal Science and Biotechnology 5(1), 53.
| Crossref | Google Scholar | PubMed |
Chang G, Mouillet JF, Mishima T, et al. (2017) Expression and trafficking of placental microRNAs at the feto-maternal interface. The FASEB Journal 31(7), 2760-2770.
| Crossref | Google Scholar | PubMed |
Chankeaw W, Lignier S, Richard C, et al. (2021) Analysis of the transcriptome of bovine endometrial cells isolated by laser micro-dissection (1): specific signatures of stromal, glandular and luminal epithelial cells. BMC Genomics 22(1), 451.
| Crossref | Google Scholar | PubMed |
Chavan AR, Griffith OW, Stadtmauer DJ, et al. (2021) Evolution of embryo implantation was enabled by the origin of decidual stromal cells in eutherian mammals. Molecular Biology and Evolution 38(3), 1060-1074.
| Crossref | Google Scholar |
Cheredath A, Uppangala S, Asha CS, et al. (2023) Combining machine learning with metabolomic and embryologic data improves embryo implantation prediction. Reproductive Sciences 30(3), 984-994.
| Crossref | Google Scholar | PubMed |
Chevalier NR, Gazquez E, Bidault L, et al. (2016) How tissue mechanical properties affect enteric neural crest cell migration. Scientific Reports 6(1), 20927.
| Crossref | Google Scholar |
Christmas MJ, Kaplow IM, Genereux DP, et al. (2023) Evolutionary constraint and innovation across hundreds of placental mammals. Science 380(6643), eabn3943.
| Crossref | Google Scholar |
Colquitt RB, Colquhoun DA, Thiele RH (2011) In silico modelling of physiologic systems. Best Practice & Research Clinical Anaesthesiology 25(4), 499-510.
| Crossref | Google Scholar | PubMed |
Cretoiu D, Xu J, Xiao J, Cretoiu SM (2016) Telocytes and their extracellular vesicles—evidence and hypotheses. International Journal of Molecular Sciences 17, 1322.
| Crossref | Google Scholar |
Cronin JG, Turner ML, Goetze L, et al. (2012) Toll-like receptor 4 and MYD88-dependent signaling mechanisms of the innate immune system are essential for the response to lipopolysaccharide by epithelial and stromal cells of the bovine endometrium. Biology of Reproduction 86(2), 51.
| Crossref | Google Scholar | PubMed |
Cruz-Munoz W, Khokha R (2008) The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Critical Reviews in Clinical Laboratory Sciences 45(3), 291-338.
| Crossref | Google Scholar | PubMed |
Davenport KM, Ortega MS, Liu H, et al. (2023) Single-nuclei RNA sequencing (snRNA-seq) uncovers trophoblast cell types and lineages in the mature bovine placenta. Proceedings of the National Academy of Sciences of the United States of America 120(12), e2221526120.
| Crossref | Google Scholar |
De Bem THC, Tinning H, Vasconcelos EJR, et al. (2021) Endometrium on-a-chip reveals insulin- and glucose-induced alterations in the transcriptome and proteomic secretome. Endocrinology 162(6), bqab054.
| Crossref | Google Scholar |
De Clercq K, Hennes A, Vriens J (2017) Isolation of mouse endometrial epithelial and stromal cells for in vitro decidualization. Journal of Visualized Experiments: JoVE [121] 55168.
| Crossref | Google Scholar |
De Wever O, Demetter P, Mareel M, et al. (2008) Stromal myofibroblasts are drivers of invasive cancer growth. International Journal of Cancer 123(10), 2229-2238.
| Crossref | Google Scholar | PubMed |
Donker RB, Mouillet JF, Chu T, et al. (2012) The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Molecular Human Reproduction 18(8), 417-424.
| Crossref | Google Scholar | PubMed |
Donofrio G, Franceschi V, Capocefalo A, et al. (2008) Bovine endometrial stromal cells display osteogenic properties. Reproductive Biology and Endocrinology: RB&E 6, 65.
| Crossref | Google Scholar |
Díez MC, Przyborski S, Del Cerro A, et al. (2023) Generation of a novel three-dimensional scaffold-based model of the bovine endometrium. Veterinary Research Communications 47(3), 1721-1733.
| Crossref | Google Scholar |
Ealy AD, Seekford ZK (2019) Symposium review: predicting pregnancy loss in dairy cattle. Journal of Dairy Science 102(12), 11798-11804.
| Crossref | Google Scholar | PubMed |
Engler AJ, Sen S, Sweeney HL, et al. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4), 677-689.
| Crossref | Google Scholar | PubMed |
Eozenou C, Lesage-Padilla A, Mauffré V, et al. (2020) FOXL2 is a progesterone target gene in the endometrium of ruminants. International Journal of Molecular Sciences 21(4), 1478.
| Crossref | Google Scholar | PubMed |
Filant J, Spencer TE (2014) Uterine glands: biological roles in conceptus implantation, uterine receptivity and decidualization. International Journal of Developmental Biology 58(2–4), 107-116.
| Crossref | Google Scholar | PubMed |
Forde N, Lonergan P (2012) Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle? Journal of Reproduction and Development 58(2), 189-195.
| Crossref | Google Scholar | PubMed |
Forde N, O’Gorman A, Whelan H, Duffy P, O’Hara L, Kelly AK, Havlicek V, Besenfelder U, Brennan L, Lonergan P (2016) Lactation-Induced changes in metabolic status and follicular-fluid metabolomic profile in postpartum dairy cows. Reproduction, Fertility and Development 28, 1882-1892.
| Crossref | Google Scholar |
Frantz C, Stewart KM, Weaver VM (2010) The extracellular matrix at a glance. Journal of Cell Science 123(24), 4195-4200.
| Crossref | Google Scholar | PubMed |
Gray CA, Burghardt RC, Johnson GA, et al. (2002) Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124(2), 289-300.
| Crossref | Google Scholar | PubMed |
Haeger J-D, Hambruch N, Dantzer V, et al. (2015) Changes in endometrial ezrin and cytokeratin 18 expression during bovine implantation and in caruncular endometrial spheroids in vitro. Placenta 36(8), 821-831.
| Crossref | Google Scholar | PubMed |
Hendijani F (2017) Explant culture: an advantageous method for isolation of mesenchymal stem cells from human tissues. Cell Proliferation 50(2), e12334.
| Crossref | Google Scholar | PubMed |
Hromadnikova I, Kotlabova K, Ondrackova M, et al. (2013) Circulating C19MC MicroRNAs in preeclampsia, gestational hypertension, and fetal growth restriction. Mediators of Inflammation 2013, e186041.
| Crossref | Google Scholar | PubMed |
Hromadnikova I, Kotlabova K, Ivankova K, et al. (2017) First trimester screening of circulating C19MC microRNAs and the evaluation of their potential to predict the onset of preeclampsia and IUGR. PLoS ONE 12(2), e0171756.
| Crossref | Google Scholar | PubMed |
Hu G, Hao K, Ling F, et al. (2022) Establishment and characterization of a sheep endometrial epithelial cell line. Biochemical and Biophysical Research Communications 603, 63-68.
| Crossref | Google Scholar | PubMed |
Huang TTF, Kosasa T, Walker B, et al. (2021) Deep learning neural network analysis of human blastocyst expansion from time-lapse image files. Reproductive BioMedicine Online 42(6), 1075-1085.
| Crossref | Google Scholar | PubMed |
Huleihel L, Hussey GS, Naranjo JD, et al. (2016) Matrix-bound nanovesicles within ECM bioscaffolds. Science Advances 2(6), e1600502.
| Crossref | Google Scholar | PubMed |
Hume L, Edge JC, Tinning H, et al. (2023) MicroRNAs emerging coordinate with placental mammals alter pathways in endometrial epithelia important for endometrial function. iScience 26(4), 106339.
| Crossref | Google Scholar | PubMed |
Hwang JY, Maziarz J, Wagner GP, et al. (2021) Molecular evolution of CatSper in mammals and function of sperm hyperactivation in gray short-tailed opossum. Cells 10(5), 1047.
| Crossref | Google Scholar | PubMed |
Idelevich A, Vilella F (2020) Mother and embryo cross-communication. Genes 11(4), 376.
| Crossref | Google Scholar | PubMed |
Kelly P, Barry-Reidy A, Brewer A, et al. (2020) Improved filtration method to isolate pure populations of primary bovine endometrial epithelial and stromal cells for immunological studies. Veterinary Research Communications 44(1), 29-39.
| Crossref | Google Scholar | PubMed |
Kim S-M, Kim J-S (2017) A review of mechanisms of implantation. Development & Reproduction 21(4), 351-359.
| Crossref | Google Scholar | PubMed |
Kirkwood PM, Gibson DA, Smith JR, et al. (2021) Single-cell RNA sequencing redefines the mesenchymal cell landscape of mouse endometrium. FASEB Journal 35(4), e21285.
| Crossref | Google Scholar | PubMed |
Langhans SA (2018) Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Frontiers in Pharmacology 9, 6.
| Crossref | Google Scholar | PubMed |
Larsen EC, Christiansen OB, Kolte AM, et al. (2013) New insights into mechanisms behind miscarriage. BMC Medicine 11(1), 154.
| Crossref | Google Scholar |
Lee J, Kotliarova S, Kotliarov Y, et al. (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9(5), 391-403.
| Crossref | Google Scholar | PubMed |
Li X, Li Z, Hou D, et al. (2016) The bovine endometrial epithelial cells promote the differentiation of trophoblast stem-like cells to binucleate trophoblast cells. Cytotechnology 68(6), 2687-2698.
| Crossref | Google Scholar | PubMed |
Li B, Duan H, Wang S, et al. (2022) Gradient boosting machine learning model for defective endometrial receptivity prediction by macrophage-endometrium interaction modules. Frontiers in Immunology 13, 842607.
| Crossref | Google Scholar | PubMed |
Lonergan P, Fair T (2014) The ART of studying early embryo development: progress and challenges in ruminant embryo culture. Theriogenology 81(1), 49-55.
| Crossref | Google Scholar | PubMed |
Lucas ES, Vrljicak P, Muter J, et al. (2020) Recurrent pregnancy loss is associated with a pro-senescent decidual response during the peri-implantation window. Communications Biology 3, 37.
| Crossref | Google Scholar |
Luo Y, Li Z, Guo H, et al. (2017) Predicting congenital heart defects: a comparison of three data mining methods. PLoS ONE 12(5), e0177811.
| Crossref | Google Scholar | PubMed |
Lynch VJ, Nnamani MC, Kapusta A, et al. (2015) Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Reports 10(4), 551-561.
| Crossref | Google Scholar | PubMed |
López-Martínez S, Campo H, de Miguel-Gómez L, et al. (2021) A natural xenogeneic endometrial extracellular matrix hydrogel toward improving current human in vitro models and future in vivo applications. Frontiers in Bioengineering and Biotechnology 9, 639688.
| Crossref | Google Scholar | PubMed |
MacKintosh SB, Schuberth HJ, Healy LL, et al. (2013) Polarised bovine endometrial epithelial cells vectorially secrete prostaglandins and chemotactic factors under physiological and pathological conditions. Reproduction 145(1), 57-72.
| Crossref | Google Scholar | PubMed |
Mathew DJ, Peterson KD, Senn LK, Oliver MA, Ealy AD (2022) Ruminant conceptus-maternal interactions: interferon-tau and beyond. Journal of Animal Science 100(7), skac123.
| Crossref | Google Scholar | PubMed |
Miao JH, Miao KH (2018) Cardiotocographic diagnosis of fetal health based on multiclass morphologic pattern predictions using deep learning classification. International Journal of Advanced Computer Science and Applications 9(5), 1-11.
| Crossref | Google Scholar |
Mika K, Marinić M, Singh M, et al. (2021) Evolutionary transcriptomics implicates new genes and pathways in human pregnancy and adverse pregnancy outcomes. eLife 10, e69584.
| Crossref | Google Scholar | PubMed |
Mika K, Whittington CM, McAllan BM, et al. (2022) Gene expression phylogenies and ancestral transcriptome reconstruction resolves major transitions in the origins of pregnancy. eLife 11, e74297.
| Crossref | Google Scholar |
Mitko K, Ulbrich SE, Wenigerkind H, Sinowatz F, Blum H, Wolf E, Bauersachs S (2008) Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction 135(2), 225-240.
| Crossref | Google Scholar | PubMed |
Morales-Prieto DM, Favaro RR, Markert UR (2020) Placental miRNAs in feto-maternal communication mediated by extracellular vesicles. Placenta 102, 27-33.
| Crossref | Google Scholar | PubMed |
Murillo A, Muñoz M (2021) Isolation, Culture, and Characterization of Primary Bovine Endometrial, Epithelial, and Stromal Cells for 3D In Vitro Tissue Models. Methods in Molecular Biology 2273, 103-110.
| Crossref | Google Scholar | PubMed |
Nallanthighal S, Heiserman JP, Cheon D-J (2019) The role of the extracellular matrix in cancer stemness. Frontiers in Cell and Developmental Biology 7, 86.
| Crossref | Google Scholar |
Nolan J, Pearce OMT, Screen HRC, Knight MM, Verbruggen SW (2023) Organ-on-a-chip and microfluidic platforms for oncology in the UK. Cancers 15(3), 635.
| Crossref | Google Scholar | PubMed |
O’Connor BB, Pope BD, Peters MM, et al. (2020) The role of extracellular matrix in normal and pathological pregnancy: future applications of microphysiological systems in reproductive medicine. Experimental Biology and Medicine 245(13), 1163-1174.
| Crossref | Google Scholar | PubMed |
Passaro C, Tutt D, Mathew DJ, et al. (2018) Blastocyst-induced changes in the bovine endometrial transcriptome. Reproduction 156(3), 219-229.
| Crossref | Google Scholar | PubMed |
Pinzón-Arteaga CA, Wang Y, Wei Y, et al. (2023) Bovine blastocyst-like structures derived from stem cell cultures. Cell Stem Cell 30(5), 611-616.e7.
| Crossref | Google Scholar | PubMed |
Pun S, Haney LC, Barrile R (2021) Modelling human physiology on-chip: historical perspectives and future directions. Micromachines 12(10), 1250.
| Crossref | Google Scholar | PubMed |
Qadan MA, Piuzzi NS, Boehm C, Bova W, Moos M, Midura RJ, Hascall VC, Malcuit C, Muschler GF (2018) Variation in primary and culture-expanded cells derived from connective tissue progenitors in human bone marrow space, bone trabecular surface and adipose tissue. Cytotherapy 20(3), 343-360.
| Crossref | Google Scholar |
Rabaglino MB, Salilew-Wondim D, Zolini A, et al. (2023) Machine-learning methods applied to integrated transcriptomic data from bovine blastocysts and elongating conceptuses to identify genes predictive of embryonic competence. The FASEB Journal 37(3), e22809.
| Crossref | Google Scholar | PubMed |
Reese ST, Franco GA, Poole RK, et al. (2020) Pregnancy loss in beef cattle: a meta-analysis. Animal Reproduction Science 212, 106251.
| Crossref | Google Scholar | PubMed |
Richter M, Piwocka O, Musielak M, et al. (2021) From donor to the lab: a fascinating journey of primary cell lines. Frontiers in Cell and Developmental Biology 9, 711381.
| Crossref | Google Scholar |
Rink BE, Amilon KR, Esteves CL, et al. (2017) Isolation and characterization of equine endometrial mesenchymal stromal cells. Stem Cell Research & Therapy 8(1), 166.
| Crossref | Google Scholar | PubMed |
Sajeesh S, Broekelman T, Mecham RP, et al. (2020) Stem cell derived extracellular vesicles for vascular elastic matrix regenerative repair. Acta Biomaterialia 113, 267-278.
| Crossref | Google Scholar | PubMed |
Sakurai T, Bai H, Bai R, et al. (2012) Coculture system that mimics in vivo attachment processes in bovine trophoblast cells. Biology of Reproduction 87(3), 60.
| Crossref | Google Scholar | PubMed |
Sanderson RD, Bandari SK, Vlodavsky I (2019) Proteases and glycosidases on the surface of exosomes: newly discovered mechanisms for extracellular remodeling. Matrix Biology: Journal of the International Society for Matrix Biology 75–76, 160-169.
| Crossref | Google Scholar | PubMed |
Scatolin GN, Ming H, Wang Y, et al. (2023) Single-cell transcriptional landscapes of bovine peri-implantation development. bioRxiv 2023.06.13.544813.
| Crossref | Google Scholar | PubMed |
Schmidt S, Friedl P (2010) Interstitial cell migration: integrin-dependent and alternative adhesion mechanisms. Cell and Tissue Research 339(1), 83-92.
| Crossref | Google Scholar | PubMed |
Scolari SC, Pugliesi G, Strefezzi RF, et al. (2016) Dynamic remodeling of endometrial extracellular matrix regulates embryo receptivity in cattle. Reproduction 153(1), 49-61.
| Crossref | Google Scholar |
Siristatidis C, Stavros S, Drakeley A, et al. (2021) Omics and artificial intelligence to improve in vitro fertilization (IVF) success: a proposed protocol. Diagnostics 11(5), 743.
| Crossref | Google Scholar | PubMed |
Spencer TE (2013) Early pregnancy: concepts, challenges, and potential solutions. Animal Frontiers 3(4), 48-55.
| Crossref | Google Scholar |
Spencer TE (2014) Biological roles of uterine glands in pregnancy. Seminars in Reproductive Medicine 32(5), 346-357.
| Crossref | Google Scholar | PubMed |
Spencer TE, Forde N, Lonergan P (2016) The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. Journal of Dairy Science 99(7), 5941-5950.
| Crossref | Google Scholar | PubMed |
Strowitzki T, Germeyer A, Popovici R, et al. (2006) The human endometrium as a fertility-determining factor. Human Reproduction Update 12(5), 617-630.
| Crossref | Google Scholar | PubMed |
Sánchez JM, Mathew DJ, Behura SK, et al. (2019) Bovine endometrium responds differentially to age-matched short and long conceptuses. Biology of Reproduction 101(1), 26-39.
| Crossref | Google Scholar | PubMed |
Taipale J, Keski-Oja J (1997) Growth factors in the extracellular matrix. The FASEB Journal 11(1), 51-59.
| Crossref | Google Scholar | PubMed |
Talbot NC, Caperna TJ, Edwards JL, et al. (2000) Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers. Biology of Reproduction 62(2), 235-247.
| Crossref | Google Scholar | PubMed |
Tan Y, Tan D, He M, et al. (2005) A model for implantation: coculture of blastocysts and uterine endometrium in mice. Biology of Reproduction 72(3), 556-561.
| Crossref | Google Scholar | PubMed |
Tavakol S, Azedi F, Hoveizi E, et al. (2018) Human endometrial stem cell isolation from endometrium and menstrual blood. Bio-Protocol 8(2), e2693.
| Crossref | Google Scholar | PubMed |
Taylor AS, Tinning H, Ovchinnikov V, et al. (2023) A burst of genomic innovation at the origin of placental mammals mediated embryo implantation. Communications Biology 6(1), 459.
| Crossref | Google Scholar |
Tinning H, Taylor A, Wang D, Constantinides B, Sutton R, Oikonomou G, Velazquez MA, Thompson P, Treumann A, O’Connell MJ, Forde N (2020) The role of CAPG in molecular communication between the embryo and the uterine endometrium: is its function conserved in species with different implantation strategies? The FASEB Journal 34(8), 11015-11029.
| Crossref | Google Scholar | PubMed |
Tkach M, Théry C (2016) Communication by extracellular vesicles: where we are and where we need to go. Cell 164(6), 1226-1232.
| Crossref | Google Scholar | PubMed |
Uyar A, Bener A, Ciray HN (2015) Predictive modeling of implantation outcome in an in vitro fertilization setting: an application of machine learning methods. Medical Decision Making 35(6), 714-725.
| Crossref | Google Scholar | PubMed |
VerMilyea M, Hall JMM, Diakiw SM, et al. (2020) Development of an artificial intelligence-based assessment model for prediction of embryo viability using static images captured by optical light microscopy during IVF. Human Reproduction 35(4), 770-784.
| Crossref | Google Scholar | PubMed |
Wang G, Johnson GA, Spencer TE, et al. (2000) Isolation, immortalization, and initial characterization of uterine cell lines: an in vitro model system for the porcine uterus. In Vitro Cellular & Developmental Biology – Animal 36(10), 650-656.
| Crossref | Google Scholar | PubMed |
Wang Y, Ming H, Yu L, et al. (2023) Establishment of bovine trophoblast stem cells. Cell Reports 42(5), 112439.
| Crossref | Google Scholar | PubMed |
Whitesides GM (2006) The origins and the future of microfluidics. Nature 442(7101), 368-373.
| Crossref | Google Scholar | PubMed |
Xiao S, Coppeta J, Rogers H, et al. (2017) A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nature Communications 8, 14584.
| Crossref | Google Scholar | PubMed |
Yiğit P, Bener A, Karabulut S (2022) Comparison of machine learning classification techniques to predict implantation success in an IVF treatment cycle. Reproductive BioMedicine Online 45(5), 923-934.
| Crossref | Google Scholar | PubMed |
Zhang S, Lin H, Kong S, et al. (2013) Physiological and molecular determinants of embryo implantation. Molecular Aspects of Medicine 34(5), 939-980.
| Crossref | Google Scholar |
