Deciphering embryo-maternal cross-talk: advanced in vitro approaches
Gislaine dos Santos; María Gemma Millán de la Blanca; Yulia Nathaly Cajas; Rosane Mazzarella; Karina Cañón-Beltrán; Maria Encina Gonzalez Martínez; Dimitrios Rizos
Abstract
Keywords
References
Abbas Y, Brunel LG, Hollinshead MS, Fernando RC, Gardner L, Duncan I, Moffett A, Best S, Turco MY, Burton GJ, Cameron RE. Generation of a three-dimensional collagen scaffold-based model of the human endometrium. Interface Focus. 2020;10(2):20190079.
Aguilera C, Velásquez AE, Gutierrez-Reinoso MA, Wong YS, Melo-Baez B, Cabezas J, Caamaño D, Navarrete F, Rojas D, Riadi G, Castro FO, Rodriguez-Alvarez L. Extracellular vesicles secreted by pre-hatching bovine embryos produced in vitro and in vivo alter the expression of ifntau-stimulated genes in bovine endometrial cells. Int J Mol Sci. 2023;24(8):7438.
Aguilera C, Wong YS, Gutierrez-Reinoso MA, Velásquez AE, Melo-Báez B, Cabezas J, Caamaño D, Navarrete F, Castro FO, Rodriguez-Alvarez LL. Embryo-maternal communication mediated by extracellular vesicles in the early stages of embryonic development is modified by in vitro conditions. Theriogenology. 2024;214:43-56.
Ahmad V, Yeddula SGR, Telugu BP, Spencer TE, Kelleher AM. Development of polarity-reversed endometrial epithelial organoids. Reproduction. 2024;167(3):167-230.
Ahn J, Yoon MJ, Hong SH, Cha H, Lee D, Koo HS, Ko JE, Lee J, Oh S, Jeon NL, Kang YJ. Three-dimensional microengineered vascularised endometrium-on-a-chip. Hum Reprod. 2021;36(10):2720-31.
Alcântara-Neto AS, Cuello C, Uzbekov R, Bauersachs S, Mermillod P, Almiñana C. Oviductal extracellular vesicles enhance porcine in vitro embryo development by modulating the embryonic transcriptome. Biomolecules. 2022;12(9):1300.
Allen RL, Wright RW Jr.
Archibong AE, Petters RM, Johnson BH. Development of porcine embryos from one- and two-cell stages to blastocysts in culture medium supplemented with porcine oviductal fluid. Biol Reprod. 1989;41(6):1076-83.
Banliat C, Le Bourhis D, Bernardi O, Tomas D, Labas V, Salvetti P, Guyonnet B, Mermillod P, Saint-Dizier M. Oviduct fluid extracellular vesicles change the phospholipid composition of bovine embryos developed in vitro. Int J Mol Sci. 2020;21(15):1-13.
Bastos NM, Ferst JG, Goulart RS, Silveira JC. The role of the oviduct and extracellular vesicles during early embryo development in bovine. Anim Reprod. 2022;19(1):e20220015.
Berg DK, Ledgard A, Donnison M, McDonald R, Henderson HV, Meier S, Juengel JL, Burke CR. The first week following insemination is the period of major pregnancy failure in pasture-grazed dairy cows. J Dairy Sci. 2022;105(11):9253-70.
Boretto M, Cox B, Noben M, Hendriks N, Fassbender A, Roose H, Amant F, Timmerman D, Tomassetti C, Vanhie A, Meuleman C, Ferrante M, Vankelecom H. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144(10):1775-86.
Borges AM, Healey GD, Sheldon IM. Explants of intact endometrium to model bovine innate immunity and inflammation
Bridi A, Sangalli JR, Nociti RP, Santos AC, Alves L, Bastos NM, Ferronato GA, Rosa PMDS, Fiorenza MF, Pugliesi G, Meirelles FV, Chiaratti MR, Silveira JC, Perecin F. Small extracellular vesicles derived from the crosstalk between early embryos and the endometrium potentially mediate corpus luteum function. Biol Reprod. 2025;112(1):54-69.
Caballero-Campo P, Domínguez F, Coloma J, Meseguer M, Remohí J, Pellicer A, Simón C. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod. 2002;8(4):375-84.
Cañón-Beltrán K, Cajas YN, Almpanis V, Egido SG, Gutierrez-Adan A, González EM, Rizos D. MicroRNA-148b secreted by bovine oviductal extracellular vesicles enhance embryo quality through BPM/TGF-beta pathway. Biol Res. 2024;57(1):11.
Chen S, Einspanier R, Schoen J. In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: estradiol and progesterone regulate differentiation, gene expression, and cellular function. Biol Reprod. 2013;89(3):54.
Chen S, Palma-Vera SE, Langhammer M, Galuska SP, Braun BC, Krause E, Lucas-Hahn A, Schoen J. An air-liquid interphase approach for modeling the early embryo-maternal contact zone. Sci Rep. 2017;7(1):42298.
Chen S, Palma-Vera SE, Kempisty B, Rucinski M, Vernunft A, Schoen J. In vitro mimicking of estrous cycle stages: dissecting the impact of estradiol and progesterone on oviduct epithelium. Endocrinology. 2018;159(9):3421-32.
Chen S, Schoen J. Air-liquid interface cell culture: from airway epithelium to the female reproductive tract. Reprod Domest Anim. 2019;54(Suppl 3):38-45.
Co JY, Margalef-Català M, Monack DM, Amieva MR. Controlling the polarity of human gastrointestinal organoids to investigate epithelial biology and infectious diseases. Nat Protoc. 2021;16(11):5171-92.
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):1163-73.
Crawford AJ, Forjaz A, Bons J, Bhorkar I, Roy T, Schell D, Queiroga V, Ren K, Kramer D, Huang W, Russo GC, Lee MH, Wu PH, Shih IM, Wang TL, Atkinson MA, Schilling B, Kiemen AL, Wirtz D. Combined assembloid modeling and 3D whole-organ mapping captures the microanatomy and function of the human fallopian tube. Sci Adv. 2024;10(39):eadp6285.
Cronin JG, Turner ML, Goetze L, Bryant CE, Sheldon IM. 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. Biol Reprod. 2012;86(2):51.
De Bem THC, Tinning H, Vasconcelos EJR, Wang D, Forde N. Endometrium on-a-chip reveals insulin- and glucose-induced alterations in the transcriptome and proteomic secretome. Endocrinology. 2021;162(6):bqab054.
Devi L, Nagargoje S, Pandey STY, Chandra V, Sharma T. Impact of uterine epithelial cells and its conditioned medium on the in vitro embryo production in buffalo (
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.
Ealy AD, Seekford ZK. Symposium review: predicting pregnancy loss in dairy cattle. J Dairy Sci. 2019;102(12):11798-804.
Edwards LJ, Batt PA, Gandolfi F, Gardner ADK. Modifications made to culture medium by bovine oviduct epithelial cells: changes to carbohydrates stimulate bovine embryo development. Mol Reprod Dev. 1997;46(2):146-54.
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.
Ellington JE, Carney EW, Farrell PB, Simkin ME, Foote RH. Bovine 1-2-cell embryo development using a simple medium in three oviduct epithelial cell coculture systems. Biol Reprod. 1990;43(1):97-104.
Ferraz MAMM, Henning HHW, Costa PF, Malda J, Melchels FP, Wubbolts R, Stout TAE, Vos PLAM, Gadella BM. Improved bovine embryo production in an oviduct-on-a-chip system: prevention of poly-spermic fertilization and parthenogenic activation. Lab Chip. 2017;17(5):905-16.
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.
Ferraz MAMM, Nagashima JB, Venzac B, Le Gac S, Songsasen N. A dog oviduct-on-a-chip model of serous tubal intraepithelial carcinoma. Sci Rep. 2020;10(1):1575.
Fitzgerald HC, Dhakal P, Behura SK, Schust DJ, Spencer TE. Self-renewing endometrial epithelial organoids of the human uterus. Proc Natl Acad Sci USA. 2019;116(46):23132-42.
Flach G, Johnson MH, Braude PR, Taylor RA, Bolton VN. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1982;1(6):681-6.
Ford MJ, Harwalkar K, Pacis AS, Maunsell H, Wang YC, Badescu D, Teng K, Yamanaka N, Bouchard M, Ragoussis J, Yamanaka Y. Oviduct epithelial cells constitute two developmentally distinct lineages that are spatially separated along the distal-proximal axis. Cell Rep. 2021;36(10):109677.
Gandolfi F, Moor RM. Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. J Reprod Fertil. 1987;81(1):23-8.
García EV, Hamdi M, Barrera AD, Sánchez-Calabuig MJ, Gutiérrez-Adán A, Rizos D. Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction. 2017;153(5):631-43.
Ghersevich S, Massa E, Zumoffen C. Oviductal secretion and gamete interaction. Reproduction. 2015;149(1):R1-14.
Gnecco JS, Pensabene V, Li DJ, Ding T, Hui EE, Bruner-Tran KL, Osteen KG. Compartmentalized culture of perivascular stroma and endothelial cells in a microfluidic model of the human endometrium. Ann Biomed Eng. 2017;45(7):1758-69.
Gnecco JS, Ding T, Smith C, Lu J, Bruner-Tran KL, Osteen KG. Hemodynamic forces enhance decidualization via endothelial-derived prostaglandin E2 and prostacyclin in a microfluidic model of the human endometrium. Hum Reprod. 2019;34(4):702-14.
Gnecco JS, Brown A, Buttrey K, Ives C, Goods BA, Baugh L, Hernandez-Gordillo V, Loring M, Isaacson KB, Griffith LG. Organoid co-culture model of the human endometrium in a fully synthetic extracellular matrix enables the study of epithelial-stromal crosstalk. Med. 2023;4(8):554-579.e9.
Gómez E, Sánchez-Calabuig MJ, Martin D, Carrocera S, Murillo A, Correia-Alvarez E, Herrero P, Canela N, Gutiérrez-Adán A, Ulbrich S, Muñoz M. In vitro cultured bovine endometrial cells recognize embryonic sex. Theriogenology. 2018;108:176-84.
Graf A, Krebs S, Heininen-Brown M, Zakhartchenko V, Blum H, Wolf E. Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Anim Reprod Sci. 2014;149(1-2):46-58.
Hamdi M, Lopera-Vásquez R, Maillo V, Sanchez-Calabuig MJ, Núnez C, Gutierrez-Adan A, Rizos D. Bovine oviductal and uterine fluid support in vitro embryo development. Reprod Fertil Dev. 2018;30(7):935-45.
Hamdi M, Sánchez JM, Fernandez-Fuertes B, Câmara DR, Bollwein H, Rizos D, Bauersachs S, Almiñana C. Oviductal extracellular vesicles miRNA cargo varies in response to embryos and their quality. BMC Genomics. 2024;25(1):520.
Hamdi M, Sánchez-Calabuig MJ, Rodríguez-Alonso B, Bagés Arnal S, Roussi K, Sturmey R, Gutiérrez-Adán A, Lonergan P, Rizos D. Gene expression and metabolic response of bovine oviduct epithelial cells to the early embryo. Reproduction. 2019;158(1):85-94.
Jackson-Bey T, Colina J, Isenberg BC, Coppeta J, Urbanek M, Kim JJ, Woodruff TK, Burdette JE, Russo A. Exposure of human fallopian tube epithelium to elevated testosterone results in alteration of cilia gene expression and beating. Hum Reprod. 2020;35(9):2086-96.
Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, Berger H, Mollenkopf HJ, Mangler M, Sehouli J, Fotopoulou C, Meyer TF. The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun. 2015;6(1):8989.
Kiani AK, Pheby D, Henehan G, Brown R, Sieving P, Sykora P, Marks R, Falsini B, Capodicasa N, Miertus S, Lorusso L, Dondossola D, Tartaglia GM, Ergoren MC, Dundar M, Michelini S, Malacarne D, Bonetti G, Dautaj A, Donato K, Medori MC, Beccari T, Samaja M, Connelly ST, Martin D, Morresi A, Bacu A, Herbst KL, Kapustin M, Stuppia L, Lumer L, Farronato G, Bertelli M. Ethical considerations regarding animal experimentation. J Prev Med Hyg. 2022;63(2, Suppl 3):E255-66.
Kim S-M, Kim J-S. A review of mechanisms of implantation. Dev Reprod. 2017;21(4):351-9.
Kwon DH, Lim B, Lee SY, Won SH, Jang G. Establishment and characterization of endometrial organoids from different placental types. BMB Rep. 2025;58(2):95-103.
Langhans SA. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol. 2018;9:6.
Larsen EC, Christiansen OB, Kolte AM, Macklon N. New insights into mechanisms behind miscarriage. BMC Med. 2013;11(1):154.
Lawson EF, Ghosh A, Blanch V, Grupen CG, Aitken RJ, Lim R, Drury HR, Baker MA, Gibb Z, Tanwar PS. Establishment and characterization of oviductal organoids from farm and companion animals†. Biol Reprod. 2023;108(6):854-65.
Leal CLV, Cañón-Beltrán K, Cajas YN, Hamdi M, Yaryes A, Millán de la Blanca MG, Beltrán-Breña P, Mazzarella R, da Silveira JC, Gutiérrez-Adán A, González EM, Rizos D. Extracellular vesicles from oviductal and uterine fluids supplementation in sequential in vitro culture improves bovine embryo quality. J Anim Sci Biotechnol. 2022;13(1):116.
Li Y, Liu C, Guo N, Cai L, Wang M, Zhu L, Li F, Jin L, Sui C. Extracellular vesicles from human Fallopian tubal fluid benefit embryo development in vitro. Hum Reprod Open. 2023;2023(2):d006.
Lonergan P, Fair T. The ART of studying early embryo development: progress and challenges in ruminant embryo culture. Theriogenology. 2014;81(1):49-55.
Lonergan P, Rizos D, Gutierrez‐Adan A, Fair T, Boland M. Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod Domest Anim. 2003;38(4):259-67.
Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltran-Brena P, Calle A, Redruello A, López-Martín S, Gutierrez-Adán A, Yañez-Mó M, Ramirez MÁ, Rizos D. Extracellular vesicles from boec in in vitro embryo development and quality. PLoS One. 2016;11(2):e0148083.
Lopera-Vasquez R, Hamdi M, Maillo V, Gutierrez-Adan A, Bermejo-Alvarez P, Ramírez MA, Yáñez-Mó M, Rizos D. Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro. Reproduction. 2017a;153(4):461-70.
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. 2017b;29(3):621-9.
Lucas E. Epigenetic effects on the embryo as a result of periconceptional environment and assisted reproduction technology. Reprod Biomed Online. 2013;27(5):477-85.
Luddi A, Pavone V, Semplici B, Governini L, Criscuoli M, Paccagnini E, Gentile M, Morgante G, De Leo V, Belmonte G, Zarovni N, Piomboni P. Organoids of human endometrium: a powerful in vitro model for the endometrium-embryo cross-talk at the implantation site. Cells. 2020;9(5):1121.
Luddi A, Pavone V, Governini L, Capaldo A, Landi C, Ietta F, Paccagnini E, Morgante G, De Leo V, Piomboni P. Emerging role of embryo secretome in the paracrine communication at the implantation site: a proof of concept. Fertil Steril. 2021;115(4):1054-62.
Mazzarella R, Cañón-Beltrán K, Cajas YN, Hamdi M, González EM, Silveira JC, Leal CLV, Rizos D. Extracellular vesicles-coupled miRNAs from oviduct and uterus modulate signaling pathways related to lipid metabolism and bovine early embryo development. J Anim Sci Biotechnol. 2024;15(1):51.
Mazzarella R, Sánchez JM, Fernandez-Fuertes B, Egido SG, McDonald M, Álvarez-Barrientos A, González E, Falcón-Pérez JM, Azkargorta M, Elortza F, González ME, Lonergan P, Rizos D. Embryo-induced changes in the protein profile of bovine oviductal extracellular vesicles. Mol Cell Proteomics. 2025;24(4):100935.
Menjivar NG, Gad A, Thompson RE, Meyers MA, Hollinshead FK, Tesfaye D. Bovine oviductal organoids: a multi-omics approach to capture the cellular and extracellular molecular response of the oviduct to heat stress. BMC Genomics. 2023;24(1):646.
Nancarrow CD, Hill JL. Co‐culture, oviduct secretion and the function of oviduct‐specific glycoproteins. Cell Biol Int. 1994;18(12):1105-14.
Passaro C, Tutt D, Mathew DJ, Sanchez JM, Browne JA, Boe-Hansen GB, Fair T, Lonergan P. Blastocyst-induced changes in the bovine endometrial transcriptome. Reproduction. 2018;156(3):219-29.
Passaro C, Tutt D, Bagés-Arnal S, Maicas C, Laguna-Barraza R, Gutierrez-Adán A, Browne JA, Rath D, Behura SK, Spencer TE, Fair T, Lonergan P. Global transcriptomic response of bovine endometrium to blastocyst-stage embryos. Reproduction. 2019;158(3):223-35.
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 (
Pranomphon T, López-Valiñas A, Almiñana C, Mahé C, Brair VL, Parnpai R, Mermillod P, Bauersachs S, Saint-Dizier M. Oviduct epithelial spheroids during in vitro culture of bovine embryos mitigate oxidative stress, improve blastocyst quality and change the embryonic transcriptome. Biol Res. 2024a;57(1):73.
Pranomphon T, Mahé C, Demattei MV, Papillier P, Vitorino Carvalho A, Reynaud K, Almiñana C, Bauersachs S, Parnpai R, Mermillod P, Saint-Dizier M. Characterization of oviduct epithelial spheroids for the study of embryo-maternal communication in cattle. Theriogenology. 2024b;217:113-26.
Qiao F, Ge H, Ma X, Ying Z, Zuo Z, Wang M, Zhang Y, Wang Y. Bovine uterus-derived exosomes improve developmental competence of somatic cell nuclear transfer embryos. Theriogenology. 2018;114:199-205.
Rawlings TM, Makwana K, Taylor DM, Molè MA, Fishwick KJ, Tryfonos M, Odendaal J, Hawkes A, Zernicka-Goetz M, Hartshorne GM, Brosens JJ, Lucas ES. Modelling the impact of decidual senescence on embryo implantation in human endometrial assembloids. eLife. 2021;10:e69603.
Reese ST, Franco GA, Poole RK, Hood R, Fernadez Montero L, Oliveira RV Fo, et al. Pregnancy loss in beef cattle: a meta-analysis. Anim Reprod Sci. 2020;212:106251.
Rizos D, Fair T, Papadopoulos S, Boland MP, Lonergan P. Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol Reprod Dev. 2002;62(3):320-7.
Santativongchai P, Klaeui CC, Kosonsiriluk S, Saqui-Salces M, Reed KM, Wileman BW, Studniski MM, Boukherroub KS. Protocol to establish turkey oviductal organoids as an in vitro model. STAR Protoc. 2024;5(4):103384.
Schmaltz-Panneau B, Cordova A, Dhorne-Pollet S, Hennequet-Antier C, Uzbekova S, Martinot E, Doret S, Martin P, Mermillod P, Locatelli Y. Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture. Anim Reprod Sci. 2014;149(3-4):103-16.
Schmaltz-Panneau B, Locatelli Y, Uzbekova S, Perreau C, Mermillod P. Bovine oviduct epithelial cells dedifferentiate partly in culture, while maintaining their ability to improve early embryo development rate and quality. Reprod Domest Anim. 2015;50(5):719-29.
Sidrat T, Khan AA, Joo MD, Wei Y, Lee KL, Xu L, Kong IK. Bovine oviduct epithelial cell-derived culture media and exosomes improve mitochondrial health by restoring metabolic flux during pre-implantation development. Int J Mol Sci. 2020;21(20):1-22.
Simintiras CA, Dhakal P, Ranjit C, Fitzgerald HC, Balboula AZ, Spencer TE. Capture and metabolomic analysis of the human endometrial epithelial organoid secretome. Proc Natl Acad Sci USA. 2021;118(15):e2026804118.
Spencer TE. Early pregnancy: concepts, challenges, and potential solutions. Anim Front. 2013;3(4):48-55.
Sponchiado M, Marei WFA, Beemster GTS, Bols PEJ, Binelli M, Leroy JLMR. Molecular interactions at the bovine embryo-endometrial epithelium interface. Reproduction. 2020;160(6):887-903.
Talukder AK, Rashid MB, Yousef MS, Kusama K, Shimizu T, Shimada M, Suarez SS, Imakawa K, Miyamoto A. Oviduct epithelium induces interferon-tau in bovine Day-4 embryos, which generates an anti-inflammatory response in immune cells. Sci Rep. 2018;8(1):7850.
Taylor DM, Ray PF, Ao A, Winston RML, Handyside AH. Paternal transcripts for glucose-6-phosphate dehydrogenase and adenosine deaminase are first detectable in the human preimplantation embryo at the three- to four-cell stage. Mol Reprod Dev. 1997;48(4):442-8.
Thompson JGE, Simpson AC, Pugh PA, Donnelly PE, Tervit HR. Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil. 1990;89(2):573-8.
Thompson RE, Meyers MA, Veeramachaneni DNR, Pukazhenthi BS, Hollinshead FK. Equine oviductal organoid generation and cryopreservation. Methods Protoc. 2022;5(3):51.
Thompson RE, Meyers MA, Premanandan C, Hollinshead FK. Generation and cryopreservation of feline oviductal organoids. Theriogenology. 2023;196:167-73.
Tinning H, Vasconcelos EJR, Wang D, Forde N. A bovine 3D endometrium-on-a-chip reveals the role of conceptus-derived proteins, CAPG and PDI, in conceptus-endometrial communication. Biol Reprod. 2025;113(1):61-82.
Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, Hollinshead M, Marsh SGE, Brosens JJ, Critchley HO, Simons BD, Hemberger M, Koo BK, Moffett A, Burton GJ. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol. 2017;19(5):568-77.
Ulbrich SE, Zitta K, Hiendleder S, Wolf E. In vitro systems for intercepting early embryo-maternal cross-talk in the bovine oviduct. Theriogenology. 2010;73(6):802-16.
van der Sanden SMG, Sachs N, Koekkoek SM, Koen G, Pajkrt D, Clevers H, Wolthers KC. Enterovirus 71 infection of human airway organoids reveals VP1-145 as a viral infectivity determinant article. Emerg Microbes Infect. 2018;7(1):84.
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.
Vassena R, Boué S, González-Roca E, Aran B, Auer H, Veiga A, Belmonte JCI. Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development. 2011;138(17):3699-709.
Wang M, Zhu T, Liu C, Jin L, Fei P, Zhang B. Oviduct-mimicking microfluidic chips decreased the ROS concentration in the in vitro fertilized embryos of CD-1 mice. Biomed Pharmacother. 2022;154:113567.
Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PLJ, 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.
Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, Olalekan SA, McKinnon KE, Dokic D, Rashedi AS, Haisenleder DJ, Malpani SS, Arnold-Murray CA, Chen K, Jiang M, Bai L, Nguyen CT, Zhang J, Laronda MM, Hope TJ, Maniar KP, Pavone ME, Avram MJ, Sefton EC, Getsios S, Burdette JE, Kim JJ, Borenstein JT, Woodruff TK. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nat Commun. 2017;8(1):14584.
Xie Y, Park ES, Xiang D, Li Z. Long-term organoid culture reveals enrichment of organoid-forming epithelial cells in the fimbrial portion of mouse fallopian tube. Stem Cell Res. 2018;32:51-60.
Zha D, Rayamajhi S, Sipes J, Russo A, Pathak HB, Li K, Sardiu ME, Bantis LE, Mitra A, Puri RV, Trinidad CV, Cain BP, Isenberg BC, Coppeta J, MacLaughlan S, Godwin AK, Burdette JE. Proteomic profiling of fallopian tube-derived extracellular vesicles using a microfluidic tissue-on-chip system. Bioengineering. 2023;10(4):423.
Submitted date:
05/08/2025
Accepted date:
07/07/2025
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email