{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,8]],"date-time":"2026-02-08T16:12:47Z","timestamp":1770567167927,"version":"3.49.0"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,1,29]],"date-time":"2024-01-29T00:00:00Z","timestamp":1706486400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p><jats:bold>Background:<\/jats:bold> During the process of elongation, the embryo increases in size within the uterus, while the extra-embryonic tissues (EETs) develop and differentiate in preparation for implantation. As it grows, the ovoid embryo transforms into a tubular form first and then a filamentous form. This process is directed by numerous genes and pathways, the expression of which may be altered in the case of developmental irregularities such as when the conceptus is shorter than expected or when the embryo develops after splitting. In bovines, efforts to understand the molecular basis of elongation have employed trophoblastic vesicles (TVs)\u2014short tubular EET pieces that lack an embryo\u2014which also elongate <jats:italic>in vivo<\/jats:italic>. To date, however, we lack molecular analyses of TVs at the ovoid or filamentous stages that might shed light on the expression changes involved.<\/jats:p><jats:p><jats:bold>Methods:<\/jats:bold> Following <jats:italic>in vivo<\/jats:italic> development, we collected bovine conceptuses from the ovoid (D12) to filamentous stages (D18), sectioned them into small pieces with or without their embryonic disc (ED), and then, transferred them to a receptive bovine uterus to assess their elongation abilities. We also grew spherical blastocysts <jats:italic>in vitro<\/jats:italic> up to D8 and subjected them to the same treatment. Then, we assessed the differences in gene expression between different samples and fully elongating controls at different stages of elongation using a bovine array (10 K) and an extended qPCR array comprising 224 genes across 24 pathways.<\/jats:p><jats:p><jats:bold>Results:<\/jats:bold><jats:italic>In vivo<\/jats:italic>, TVs elongated more or less depending on the stage at which they had been created and the time spent <jats:italic>in utero<\/jats:italic>. Their daily elongation rates differed from control EET, with the rates of TVs sometimes resembling those of earlier-stage EET. Overall, the molecular signatures of TVs followed a similar developmental trajectory as intact EET from D12\u2013D18. However, within each stage, TVs and intact EET displayed distinct expression dynamics, some of which were shared with other short epithelial models.<\/jats:p><jats:p><jats:bold>Conclusion:<\/jats:bold> Differences between TVs and EET likely result from multiple factors, including a reduction in the length and signaling capabilities of TVs, delayed elongation from inadequate uterine signals, and modified crosstalk between the conceptus and the uterus. These findings confirm that close coordination between uterine, embryonic, and extra-embryonic tissues is required to orchestrate proper elongation and, based on the partial differentiation observed, raise questions about the presence\/absence of certain developmental cues or even their asynchronies.<\/jats:p>","DOI":"10.3389\/fphys.2024.1331098","type":"journal-article","created":{"date-parts":[[2024,1,29]],"date-time":"2024-01-29T04:37:56Z","timestamp":1706503076000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Understanding bovine embryo elongation: a transcriptomic study of trophoblastic vesicles"],"prefix":"10.3389","volume":"15","author":[{"given":"S\u00e9verine A.","family":"Degrelle","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fulin","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Denis","family":"Laloe","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christophe","family":"Richard","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel","family":"Le Bourhis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marie-No\u00eblle","family":"Rossignol","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Isabelle","family":"Hue","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2024,1,29]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"112412","DOI":"10.1016\/j.celrep.2023.112412","article-title":"Emergence of division of labor in tissues through cell interactions and spatial cues","volume":"42","author":"Adler","year":"2023","journal-title":"Cell Rep."},{"key":"B2","doi-asserted-by":"publisher","first-page":"e21904","DOI":"10.1096\/fj.202002762RR","article-title":"Deciphering two rounds of cell lineage segregations during bovine preimplantation development","volume":"35","author":"Akizawa","year":"2021","journal-title":"FASEB J."},{"key":"B3","doi-asserted-by":"publisher","first-page":"R151","DOI":"10.1530\/REP-19-0348","article-title":"Preimplantation development in ungulates: a 'menage a quatre' scenario","volume":"159","author":"Artus","year":"2020","journal-title":"Reproduction"},{"key":"B4","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/j.aninu.2015.07.005","article-title":"Select nutrients and their effects on conceptus development in mammals","volume":"1","author":"Bazer","year":"2015","journal-title":"Anim. Nutr."},{"key":"B5","doi-asserted-by":"publisher","first-page":"e56454","DOI":"10.15252\/embr.202256454","article-title":"Terminal differentiation of villus tip enterocytes is governed by distinct Tgf\u03b2 superfamily members","volume":"24","author":"Berkova","year":"2023","journal-title":"EMBO Rep."},{"key":"B6","doi-asserted-by":"publisher","first-page":"bio033282","DOI":"10.1242\/bio.033282","article-title":"Mammalian embryo comparison identifies novel pluripotency genes associated with the naive or primed state","volume":"7","author":"Bernardo","year":"2018","journal-title":"Biol. Open"},{"key":"B7","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1530\/jrf.0.0590205","article-title":"Collection, description and transfer of embryos from cattle 10--16 days after oestrus","volume":"59","author":"Betteridge","year":"1980","journal-title":"J. Reprod. Fertil."},{"key":"B8","doi-asserted-by":"publisher","first-page":"3639","DOI":"10.1242\/dev.133132","article-title":"Regulation and plasticity of intestinal stem cells during homeostasis and regeneration","volume":"143","author":"Beumer","year":"2016","journal-title":"Development"},{"key":"B9","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1530\/REP-07-0355","article-title":"Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation","volume":"135","author":"Blomberg","year":"2008","journal-title":"Reproduction"},{"key":"B10","doi-asserted-by":"publisher","first-page":"2048","DOI":"10.1095\/biolreprod.103.025916","article-title":"Post hatching development: a novel system for extended in vitro culture of bovine embryos","volume":"71","author":"Brandao","year":"2004","journal-title":"Biol. Reprod."},{"key":"B11","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1095\/biolreprod.114.123877","article-title":"Peroxisome proliferator activator receptor gamma (PPARG) regulates conceptus elongation in sheep","volume":"92","author":"Brooks","year":"2015","journal-title":"Biol. Reprod."},{"key":"B12","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1071\/RD23181","article-title":"Understanding conceptus-maternal interactions: what tools do we need to develop?","volume":"36","author":"Butt","year":"2023","journal-title":"Reprod. Fertil. Dev."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1280","DOI":"10.1093\/bioinformatics\/bti141","article-title":"PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order","volume":"21","author":"Caraux","year":"2005","journal-title":"Bioinformatics"},{"key":"B14","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1530\/REP-09-0152","article-title":"Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium?","volume":"138","author":"Clemente","year":"2009","journal-title":"Reproduction"},{"key":"B15","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.1095\/biolreprod62.6.1677","article-title":"Onset of the first S-phase is determined by a paternal effect during the G1-phase in bovine zygotes","volume":"62","author":"Comizzoli","year":"2000","journal-title":"Biol. Reprod."},{"key":"B16","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1016\/j.ydbio.2005.09.043","article-title":"Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts","volume":"288","author":"Degrelle","year":"2005","journal-title":"Dev. Biol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"e38309","DOI":"10.1371\/journal.pone.0038309","article-title":"Uncoupled embryonic and extra-embryonic tissues compromise blastocyst development after somatic cell nuclear transfer","volume":"7","author":"Degrelle","year":"2012","journal-title":"PLoS One"},{"key":"B18","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1530\/REP-10-0174","article-title":"A small set of extra-embryonic genes defines a new landmark for bovine embryo staging","volume":"141","author":"Degrelle","year":"","journal-title":"Reproduction"},{"key":"B70","doi-asserted-by":"publisher","first-page":"917","DOI":"10.1016\/j.placenta.2011.08.014","article-title":"Expression and localization of DLX3, PPARG and SP1 in bovine trophoblast during binucleated cell differentiation","volume":"32","author":"Degrelle","year":"","journal-title":"Placenta"},{"key":"B19","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1051\/rnd:19860609","article-title":"Experimental studies on the elongation of the Ewe blastocyst","volume":"26","author":"Flechon","year":"1986","journal-title":"Reprod. Nutr. Dev."},{"key":"B20","doi-asserted-by":"publisher","first-page":"e100010","DOI":"10.1371\/journal.pone.0100010","article-title":"Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle","volume":"9","author":"Forde","year":"2014","journal-title":"PLoS One"},{"key":"B21","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1242\/dev.28.2.279","article-title":"An investigation of inner cell mass and trophoblast tissues following their isolation from the mouse blastocyst","volume":"28","author":"Gardner","year":"1972","journal-title":"J. Embryol. Exp. Morphol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1038\/s41576-020-0239-7","article-title":"Gene regulatory programmes of tissue regeneration","volume":"21","author":"Goldman","year":"2020","journal-title":"Nat. Rev. Genet."},{"key":"B23","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1530\/rep.0.1240289","article-title":"Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation","volume":"124","author":"Gray","year":"2002","journal-title":"Reproduction"},{"key":"B24","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1002\/ar.1091320308","article-title":"Observations on the morphogenesis and histochemistry of the bovine preattachment placenta between 16 and 33 days of gestation","volume":"132","author":"Greenstein","year":"1958","journal-title":"Anat. Rec."},{"key":"B25","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1530\/jrf.0.0700533","article-title":"Maintenance of the corpus luteum after uterine transfer of trophoblastic vesicles to cyclic cows and ewes","volume":"70","author":"Heyman","year":"1984","journal-title":"J. Reprod. Fertil."},{"key":"B26","doi-asserted-by":"publisher","first-page":"409","DOI":"10.15252\/embj.201695690","article-title":"ANGPTL2 expression in the intestinal stem cell niche controls epithelial regeneration and homeostasis","volume":"36","author":"Horiguchi","year":"2017","journal-title":"EMBO J."},{"key":"B27","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1093\/icb\/icu067","article-title":"The Drosophila egg chamber-a new spin on how tissues elongate","volume":"54","author":"Horne-Badovinac","year":"2014","journal-title":"Integr. Comp. Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1530\/REP-18-0439","article-title":"Different pre-implantation phenotypes of bovine blastocysts produced in vitro","volume":"157","author":"Hue","year":"2018","journal-title":"Reproduction"},{"key":"B29","doi-asserted-by":"publisher","first-page":"e0127330","DOI":"10.1371\/journal.pone.0127330","article-title":"Primary bovine extra-embryonic cultured cells: a new resource for the study of in vivo peri-implanting phenotypes and mesoderm formation","volume":"10","author":"Hue","year":"2015","journal-title":"PLoS One"},{"key":"B30","doi-asserted-by":"publisher","first-page":"944370","DOI":"10.3389\/fvets.2022.944370","article-title":"New roles for EVs, miRNA and lncRNA in bovine embryo implantation","volume":"9","author":"Imakawa","year":"2022","journal-title":"Front. Vet. Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"112860","DOI":"10.1016\/j.celrep.2023.112860","article-title":"Single-cell transcriptomic characterization of sheep conceptus elongation and implantation","volume":"42","author":"Jia","year":"2023","journal-title":"Cell Rep."},{"key":"B32","doi-asserted-by":"publisher","first-page":"e34110","DOI":"10.1371\/journal.pone.0034110","article-title":"Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo","volume":"7","author":"Khan","year":"2012","journal-title":"PLoS One"},{"key":"B33","doi-asserted-by":"publisher","first-page":"R1098","DOI":"10.1016\/j.cub.2021.07.078","article-title":"Dynamic changes in epithelial cell packing during tissue morphogenesis","volume":"31","author":"Lemke","year":"2021","journal-title":"Curr. Biol."},{"key":"B71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2020\/9210748","article-title":"Comparative study of PPAR\u03b3 targets in human extravillous and villous cytotrophoblasts","volume":"2020","author":"Liu","year":"2020","journal-title":"PPAR Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1530\/rep.0.1250607","article-title":"Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos","volume":"125","author":"Maddox-Hyttel","year":"2003","journal-title":"Reproduction"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1095\/biolreprod.111.092643","article-title":"RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation","volume":"85","author":"Mamo","year":"2011","journal-title":"Biol. Reprod."},{"key":"B36","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.anireprosci.2012.08.011","article-title":"Transcriptomic changes in the bovine conceptus between the blastocyst stage and initiation of implantation","volume":"134","author":"Mamo","year":"2012","journal-title":"Anim. Reprod. Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"skac123","DOI":"10.1093\/jas\/skac123","article-title":"Ruminant conceptus-maternal interactions: interferon-tau and beyond","volume":"100","author":"Mathew","year":"2022","journal-title":"J. Anim. Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1051\/rnd:19970202","article-title":"Beneficial effects of Vero cells for developing IVF bovine eggs in two different coculture systems","volume":"37","author":"Menck","year":"1997","journal-title":"Reprod. Nutr. Dev."},{"key":"B39","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.trsl.2016.06.002","article-title":"The gut microbiota and inflammatory bowel diseases","volume":"179","author":"Miyoshi","year":"2017","journal-title":"Transl. Res."},{"key":"B40","doi-asserted-by":"publisher","first-page":"E1749","DOI":"10.1073\/pnas.1721191115","article-title":"Uterine influences on conceptus development in fertility-classified animals","volume":"115","author":"Moraes","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B41","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1262\/jrd.20222","article-title":"Production of trophoblastic vesicles derived from Day 7 and 8 blastocysts of in vitro origin and the effect of intrauterine transfer on the interestrous intervals in Japanese black heifers","volume":"55","author":"Nagai","year":"2009","journal-title":"J. Reprod. Dev."},{"key":"B42","doi-asserted-by":"publisher","first-page":"9763","DOI":"10.3168\/jds.2023-23399","article-title":"Transcriptome changes associated with elongation of bovine conceptuses II: differentially expressed transcripts in the endometrium on day 17 after insemination","volume":"106","author":"Peixoto","year":"2023","journal-title":"J. Dairy Sci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"680539","DOI":"10.3389\/fvets.2021.680539","article-title":"Lineage differentiation markers as a proxy for embryo viability in farm ungulates","volume":"8","author":"Perez-Gomez","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1530\/REP-11-0374","article-title":"Trophoblast development","volume":"143","author":"Pfeffer","year":"2012","journal-title":"Reproduction"},{"key":"B45","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1017\/S0967199417000090","article-title":"Gene expression analysis of bovine embryonic disc, trophoblast and parietal hypoblast at the start of gastrulation","volume":"25","author":"Pfeffer","year":"2017","journal-title":"Zygote"},{"key":"B46","doi-asserted-by":"publisher","first-page":"bio037937","DOI":"10.1242\/bio.037937","article-title":"Physiological profile of undifferentiated bovine blastocyst-derived trophoblasts","volume":"8","author":"Pillai","year":"2019","journal-title":"Biol. Open"},{"key":"B47","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1095\/biolreprod39.5.999","article-title":"Uterine asynchrony: a cause of embryonic loss","volume":"39","author":"Pope","year":"1988","journal-title":"Biol. Reprod."},{"key":"B48","doi-asserted-by":"publisher","first-page":"dev199743","DOI":"10.1242\/dev.199743","article-title":"In vitro culture of ovine embryos up to early gastrulating stages","volume":"149","author":"Ramos-Ibeas","year":"2022","journal-title":"Development"},{"key":"B49","doi-asserted-by":"publisher","first-page":"3630","DOI":"10.3168\/jds.2017-13469","article-title":"Symposium review: lipids as regulators of conceptus development: implications for metabolic regulation of reproduction in dairy cattle","volume":"101","author":"Ribeiro","year":"2018","journal-title":"J. Dairy Sci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1095\/biolreprod.115.134908","article-title":"Biology of preimplantation conceptus at the onset of elongation in dairy cows","volume":"94","author":"Ribeiro","year":"2016","journal-title":"Biol. Reprod."},{"key":"B51","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1016\/j.theriogenology.2014.12.005","article-title":"Transcervical collection of bovine embryos up to Day 21: an 8-year overview","volume":"83","author":"Richard","year":"2015","journal-title":"Theriogenology"},{"key":"B52","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1093\/biolre\/ioz060","article-title":"Bovine endometrium responds differentially to age-matched short and long conceptuses\u2020","volume":"101","author":"Sanchez","year":"2019","journal-title":"Biol. Reprod."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1062","DOI":"10.1016\/j.tcb.2018.08.001","article-title":"The intestinal stem cell niche: homeostasis and adaptations","volume":"28","author":"Santos","year":"2018","journal-title":"Trends Cell Biol."},{"key":"B54","article-title":"Single-cell transcriptional landscapes of bovine peri-implantation development","author":"Scatolin","year":"2023"},{"key":"B55","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1146\/annurev-animal-020518-115321","article-title":"Development and function of uterine glands in domestic animals","volume":"7","author":"Spencer","year":"2019","journal-title":"Annu. Rev. Anim. Biosci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1530\/jrf.0.1110191","article-title":"Support for the development of bovine embryos in vitro by secretions of bovine trophoblastic vesicles derived in vitro","volume":"111","author":"Stojkovic","year":"1997","journal-title":"J. Reprod. Fertil."},{"key":"B72","doi-asserted-by":"publisher","first-page":"1816","DOI":"10.1111\/j.1365-294X.2011.05317.x","article-title":"Soil sampling and isolation of extracellular DNA from large amount of starting material suitable for metabarcoding studies","volume":"21","author":"Taberlet","year":"2012","journal-title":"Mol. Ecol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1186\/1477-7827-2-77","article-title":"cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period","volume":"2","author":"Ushizawa","year":"2004","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"1253","DOI":"10.1016\/j.theriogenology.2004.01.007","article-title":"Rapid growth and elongation of bovine blastocysts in vitro in a three-dimensional gel system","volume":"62","author":"Vajta","year":"2004","journal-title":"Theriogenology"},{"key":"B59","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.ydbio.2014.01.008","article-title":"Paracrine effects of embryo-derived FGF4 and BMP4 during pig trophoblast elongation","volume":"387","author":"Valdez Magana","year":"2014","journal-title":"Dev. Biol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1152\/physiolgenomics.00091.2013","article-title":"Energy and lipid metabolism gene expression of D18 embryos in dairy cows is related to dam physiological status","volume":"46","author":"Valour","year":"2014","journal-title":"Physiol. Genomics"},{"key":"B61","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/j.tcb.2021.06.007","article-title":"3D gastruloids: a novel frontier in stem cell-based in vitro modeling of mammalian gastrulation","volume":"31","author":"Van Den Brink","year":"2021","journal-title":"Trends Cell Biol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"e0129787","DOI":"10.1371\/journal.pone.0129787","article-title":"Morphological and gene expression changes in cattle embryos from hatched blastocyst to early gastrulation stages after transfer of in vitro produced embryos","volume":"10","author":"Van Leeuwen","year":"2015","journal-title":"PLoS One"},{"key":"B63","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.theriogenology.2016.08.014","article-title":"Embryo splitting affects the transcriptome during elongation stage of in vitro-produced bovine blastocysts","volume":"87","author":"Velasquez","year":"2017","journal-title":"Theriogenology"},{"key":"B64","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1071\/RD22210","article-title":"Secreted metabolome of porcine blastocysts encapsulated within in vitro 3D alginate hydrogel culture systems undergoing morphological changes provides insights into specific mechanisms involved in the initiation of porcine conceptus elongation","volume":"35","author":"Walsh","year":"2023","journal-title":"Reprod. Fertil. Dev."},{"key":"B65","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.anireprosci.2010.12.001","article-title":"A review of the causes of poor fertility in high milk producing dairy cows","volume":"123","author":"Walsh","year":"2011","journal-title":"Anim. Reprod. Sci."},{"key":"B66","doi-asserted-by":"publisher","first-page":"2261","DOI":"10.1242\/dev.135400","article-title":"Generation of intestinal surface: an absorbing tale","volume":"143","author":"Walton","year":"2016","journal-title":"Development"},{"key":"B67","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1038\/nmeth.3016","article-title":"A method to recapitulate early embryonic spatial patterning in human embryonic stem cells","volume":"11","author":"Warmflash","year":"2014","journal-title":"Nat. Methods"},{"key":"B68","doi-asserted-by":"publisher","first-page":"5859","DOI":"10.1016\/j.cell.2023.11.008","article-title":"Dissecting embryonic and extraembryonic lineage crosstalk with stem cell co-culture","volume":"186","author":"Wei","year":"2023","journal-title":"Cell"},{"key":"B69","doi-asserted-by":"publisher","first-page":"110666","DOI":"10.1016\/j.celrep.2022.110666","article-title":"Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction","volume":"39","author":"Weng","year":"2022","journal-title":"Cell Rep."}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2024.1331098\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,29]],"date-time":"2024-01-29T04:38:01Z","timestamp":1706503081000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2024.1331098\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,29]]},"references-count":72,"alternative-id":["10.3389\/fphys.2024.1331098"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2024.1331098","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,29]]},"article-number":"1331098"}}