Molecular factors driving the development of bovine embryos and embryo-like structures
Zongliang Jiang
Abstract
Keywords
References
Banliat C, Mahe C, Lavigne R, Com E, Pineau C, Labas V, Guyonnet B, Mermillod P, Saint-Dizier M. Dynamic changes in the proteome of early bovine embryos developed in vivo. Front Cell Dev Biol. 2022a;10:863700.
Banliat C, Mahe C, Lavigne R, Com E, Pineau C, Labas V, Guyonnet B, Mermillod P, Saint-Dizier M. The proteomic analysis of bovine embryos developed in vivo or in vitro reveals the contribution of the maternal environment to early embryo. BMC Genomics. 2022b;23(1):839.
Becker K, Bluhm A, Casas-Vila N, Dinges N, Dejung M, Sayols S, Kreutz C, Roignant JY, Butter F, Legewie S. Quantifying post-transcriptional regulation in the development of
Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6-21.
Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K, Izpisua Belmonte JC, Ross PJ. Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proc Natl Acad Sci USA. 2018;115(9):2090-5.
Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A. Capture of authentic embryonic stem cells from rat blastocysts. Cell. 2008;135(7):1287-98.
Canizo JR, Ynsaurralde Rivolta AE, Vazquez Echegaray C, Suva M, Alberio V, Aller JF, Guberman AS, Salamone DF, Alberio RH, Alberio R. A dose-dependent response to MEK inhibition determines hypoblast fate in bovine embryos. BMC Dev Biol. 2019;19(1):13.
Cuthbert JM, Russell SJ, Polejaeva IA, Meng Q, White KL, Benninghoff AD. Dynamics of small non-coding RNAs in bovine scNT embryos through the maternal-to-embryonic transitiondagger. Biol Reprod. 2021;105(4):918-33.
Cuthbert JM, Russell SJ, White KL, Benninghoff AD. The maternal-to-zygotic transition in bovine in vitro-fertilized embryos is associated with marked changes in small non-coding RNAsdagger. Biol Reprod. 2019;100(2):331-50.
Deutsch DR, Frohlich T, Otte KA, Beck A, Habermann FA, Wolf E, Arnold GJ. Stage-specific proteome signatures in early bovine embryo development. J Proteome Res. 2014;13(10):4363-76.
Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim. 2008;43(Suppl 2):260-7.
Duan JE, Jiang ZC, Alqahtani F, Mandoiu I, Dong H, Zheng X, Marjani SL, Chen J, Tian XC. Methylome dynamics of bovine gametes and in vivo early embryos. Front Genet. 2019;10:512.
Dupont C, Schaffers OJM, Tan BF, Merzouk S, Bindels EM, Zwijsen A, Huylebroeck D, Gribnau J. Efficient generation of ETX embryoids that recapitulate the entire window of murine egg cylinder development. Sci Adv. 2023;9(3):eadd2913.
Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigó R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW, Reymond A, Rijnkels M, Skow LC, Zdobnov EM, Schook L, Womack J, Alioto T, Antonarakis SE, Astashyn A, Chapple CE, Chen HC, Chrast J, Câmara F, Ermolaeva O, Henrichsen CN, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Kokocinski F, Landrum M, Maglott D, Pruitt K, Sapojnikov V, Searle SM, Solovyev V, Souvorov A, Ucla C, Wyss C, Anzola JM, Gerlach D, Elhaik E, Graur D, Reese JT, Edgar RC, McEwan JC, Payne GM, Raison JM, Junier T, Kriventseva EV, Eyras E, Plass M, Donthu R, Larkin DM, Reecy J, Yang MQ, Chen L, Cheng Z, Chitko-McKown CG, Liu GE, Matukumalli LK, Song J, Zhu B, Bradley DG, Brinkman FS, Lau LP, Whiteside MD, Walker A, Wheeler TT, Casey T, German JB, Lemay DG, Maqbool NJ, Molenaar AJ, Seo S, Stothard P, Baldwin CL, Baxter R, Brinkmeyer-Langford CL, Brown WC, Childers CP, Connelley T, Ellis SA, Fritz K, Glass EJ, Herzig CT, Iivanainen A, Lahmers KK, Bennett AK, Dickens CM, Gilbert JG, Hagen DE, Salih H, Aerts J, Caetano AR, Dalrymple B, Garcia JF, Gill CA, Hiendleder SG, Memili E, Spurlock D, Williams JL, Alexander L, Brownstein MJ, Guan L, Holt RA, Jones SJ, Marra MA, Moore R, Moore SS, Roberts A, Taniguchi M, Waterman RC, Chacko J, Chandrabose MM, Cree A, Dao MD, Dinh HH, Gabisi RA, Hines S, Hume J, Jhangiani SN, Joshi V, Kovar CL, Lewis LR, Liu YS, Lopez J, Morgan MB, Nguyen NB, Okwuonu GO, Ruiz SJ, Santibanez J, Wright RA, Buhay C, Ding Y, Dugan-Rocha S, Herdandez J, Holder M, Sabo A, Egan A, Goodell J, Wilczek-Boney K, Fowler GR, Hitchens ME, Lozado RJ, Moen C, Steffen D, Warren JT, Zhang J, Chiu R, Schein JE, Durbin KJ, Havlak P, Jiang H, Liu Y, Qin X, Ren Y, Shen Y, Song H, Bell SN, Davis C, Johnson AJ, Lee S, Nazareth LV, Patel BM, Pu LL, Vattathil S, Williams RL Jr, Curry S, Hamilton C, Sodergren E, Wheeler DA, Barris W, Bennett GL, Eggen A, Green RD, Harhay GP, Hobbs M, Jann O, Keele JW, Kent MP, Lien S, McKay SD, McWilliam S, Ratnakumar A, Schnabel RD, Smith T, Snelling WM, Sonstegard TS, Stone RT, Sugimoto Y, Takasuga A, Taylor JF, Van Tassell CP, Macneil MD, Abatepaulo AR, Abbey CA, Ahola V, Almeida IG, Amadio AF, Anatriello E, Bahadue SM, Biase FH, Boldt CR, Carroll JA, Carvalho WA, Cervelatti EP, Chacko E, Chapin JE, Cheng Y, Choi J, Colley AJ, de Campos TA, De Donato M, Santos IK, de Oliveira CJ, Deobald H, Devinoy E, Donohue KE, Dovc P, Eberlein A, Fitzsimmons CJ, Franzin AM, Garcia GR, Genini S, Gladney CJ, Grant JR, Greaser ML, Green JA, Hadsell DL, Hakimov HA, Halgren R, Harrow JL, Hart EA, Hastings N, Hernandez M, Hu ZL, Ingham A, Iso-Touru T, Jamis C, Jensen K, Kapetis D, Kerr T, Khalil SS, Khatib H, Kolbehdari D, Kumar CG, Kumar D, Leach R, Lee JC, Li C, Logan KM, Malinverni R, Marques E, Martin WF, Martins NF, Maruyama SR, Mazza R, McLean KL, Medrano JF, Moreno BT, Moré DD, Muntean CT, Nandakumar HP, Nogueira MF, Olsaker I, Pant SD, Panzitta F, Pastor RC, Poli MA, Poslusny N, Rachagani S, Ranganathan S, Razpet A, Riggs PK, Rincon G, Rodriguez-Osorio N, Rodriguez-Zas SL, Romero NE, Rosenwald A, Sando L, Schmutz SM, Shen L, Sherman L, Southey BR, Lutzow YS, Sweedler JV, Tammen I, Telugu BP, Urbanski JM, Utsunomiya YT, Verschoor CP, Waardenberg AJ, Wang Z, Ward R, Weikard R, Welsh TH Jr, White SN, Wilming LG, Wunderlich KR, Yang J, Zhao FQ. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science. 2009;324(5926):522-8.
Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292(5819):154-6.
Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol. 2004;5(10):827-35.
Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci USA. 2014;111(11):4139-44.
Halstead MM, Ma X, Zhou C, Schultz RM, Ross PJ. Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation. Nat Commun. 2020;11(1):4654.
Hasler JF. Forty years of embryo transfer in cattle: a review focusing on the journal Theriogenology, the growth of the industry in North America, and personal reminisces. Theriogenology. 2014;81(1):152-69.
Hu L, Liu S, Peng Y, Ge R, Su R, Senevirathne C, Harada BT, Dai Q, Wei J, Zhang L, Hao Z, Luo L, Wang H, Wang Y, Luo M, Chen M, Chen J, He C. m(6)A RNA modifications are measured at single-base resolution across the mammalian transcriptome. Nat Biotechnol. 2022;40(8):1210-9.
Iyyappan R, Niu Y, Ming H, Pajdzik K, Rakestraw NR, Jain PK, He C, Zong C, Jiang Z. Single-nucleotide resolution epitranscriptomic profiling uncovers dynamic m6A regulation in bovine preimplantation development. bioRxiv. 2025. Forthcoming. PMid:40672241.
Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245-54.
Jiang Z, Sun J, Dong H, Luo O, Zheng X, Obergfell C, Tang Y, Bi J, O’Neill R, Ruan Y, Chen J, Tian XC. Transcriptional profiles of bovine in vivo pre-implantation development. BMC Genomics. 2014;15(1):756.
Jiang Z, Lin J, Dong H, Zheng X, Marjani SL, Duan J, Ouyang Z, Chen J, Tian XC. DNA methylomes of bovine gametes and in vivo produced preimplantation embryos. Biol Reprod. 2018;99(5):949-59.
Jiang Z. Molecular and cellular programs underlying the development of bovine pre-implantation embryos. Reprod Fertil Dev. 2023;36(2):34-42.
Kues WA, Sudheer S, Herrmann D, Carnwath JW, 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):19768-73.
Kuijk EW, van Tol LT, Van de Velde H, Wubbolts R, Welling M, Geijsen N, Roelen BA. The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development. 2012;139(5):871-82.
Langkabel J, Horne A, Bonaguro L, Holsten L, Hesse T, Knaus A, Riedel Y, Becker M, Handler K, Elmzzahi T, Bassler K, Reusch N, Yeghiazarian LH, Pecht T, Saglam A, Ulas T, Aschenbrenner AC, Kaiser F, Kubaczka C, Schultze JL, Schorle H. Induction of Rosette-to-Lumen stage embryoids using reprogramming paradigms in ESCs. Nat Commun. 2021;12(1):7322.
Lavoie H, Gagnon J, Therrien M. ERK signalling: a master regulator of cell behaviour, life and fate. Nat Rev Mol Cell Biol. 2020;21(10):607-32.
Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature. 1993;366(6453):362-5.
Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh CL, Pera MF, Ying QL. Germline competent embryonic stem cells derived from rat blastocysts. Cell. 2008;135(7):1299-310.
Li R, Zhong C, Yu Y, Liu H, Sakurai M, Yu L, Min Z, Shi L, Wei Y, Takahashi Y, Liao HK, Qiao J, Deng H, Nunez-Delicado E, Rodriguez Esteban C, Wu J, Izpisua Belmonte JC. Generation of blastocyst-like structures from mouse embryonic and adult cell cultures. Cell. 2019;179(3):687-702.e18.
Lodewijk GA, Kozuki S, Han CJ, Topacio BR, Lee S, Nixon L, Zargari A, Knight G, Ashton R, Qi LS, Shariati SA. Self-organization of mouse embryonic stem cells into reproducible pre-gastrulation embryo models via CRISPRa programming. Cell Stem Cell. 2025;32(6):895-913.e8.
Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA. 1981;78(12):7634-8.
Ming H, Sun J, Pasquariello R, Gatenby L, Herrick JR, Yuan Y, Pinto CR, Bondioli KR, Krisher RL, Jiang Z. The landscape of accessible chromatin in bovine oocytes and early embryos. Epigenetics. 2021;16(3):300-12.
Ming H, Zhang M, Rajput S, Logsdon D, Zhu L, Schoolcraft WB, Krisher RL, Jiang Z, Yuan Y. In vitro culture alters cell lineage composition and cellular metabolism of bovine blastocystdagger. Biol Reprod. 2024;111(1):11-27.
Ming H, Scatolin GN, Ojeda-Rojas OA, Jiang Z. Establishment of bovine extraembryonic endoderm stem cells enables efficient blastoid formation. Cell Rep. 2025;44(6):115707.
Pauli A, Rinn JL, Schier AF. Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet. 2011;12(2):136-49.
Paulson EE, Fishman EL, Ma J, Schultz RM, Ross PJ. Embryonic microRNAs are essential for bovine preimplantation embryo development. Proc Natl Acad Sci USA. 2022;119(45):e2212942119.
Pinzon-Arteaga CA, Wang Y, Wei Y, Ribeiro Orsi AE, Li L, Scatolin G, Liu L, Sakurai M, Ye J, Hao M, Yu L, Li B, Jiang Z, Wu J. Bovine blastocyst-like structures derived from stem cell cultures. Cell Stem Cell. 2023;30(5):611-616.e7.
Rabaglino MB, Salilew-Wondim D, Zolini A, Tesfaye D, Hoelker M, Lonergan P, Hansen PJ. Machine-learning methods applied to integrated transcriptomic data from bovine blastocysts and elongating conceptuses to identify genes predictive of embryonic competence. FASEB J. 2023;37(3):e22809.
Rivron NC, Frias-Aldeguer J, Vrij EJ, Boisset JC, Korving J, Vivie J, Truckenmuller RK, van Oudenaarden A, van Blitterswijk CA, Geijsen N. Blastocyst-like structures generated solely from stem cells. Nature. 2018;557(7703):106-11.
Rossant J, Tam PPL. New insights into early human development: lessons for stem cell derivation and differentiation. Cell Stem Cell. 2017;20(1):18-28.
Sozen B, Cox AL, De Jonghe J, Bao M, Hollfelder F, Glover DM, Zernicka-Goetz M. Self-organization of mouse stem cells into an extended potential blastoid. Dev Cell. 2019;51(6):698-712.e8.
Stoecklein KS, Ortega MS, Spate LD, Murphy CN, Prather RS. Improved cryopreservation of in vitro produced bovine embryos using FGF2, LIF, and IGF1. PLoS One. 2021;16(2):e0243727.
Su Y, Zhu J, Salman S, Tang Y. Induced pluripotent stem cells from farm animals. J Anim Sci. 2020;98(11):skaa343.
Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Annu Rev Biochem. 2011;80(1):473-99.
Tarazi S, Aguilera-Castrejon A, Joubran C, Ghanem N, Ashouokhi S, Roncato F, Wildschutz E, Haddad M, Oldak B, Gomez-Cesar E, Livnat N, Viukov S, Lokshtanov D, Naveh-Tassa S, Rose M, Hanna S, Raanan C, Brenner O, Kedmi M, Keren-Shaul H, Lapidot T, Maza I, Novershtern N, Hanna JH. Post-gastrulation synthetic embryos generated ex utero from mouse naive ESCs. Cell. 2022;185(18):3290-3306.e25.
Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer. 2010;10(2):116-29.
Wang D, Ming H, Yang D, Tsai L-K, Wei Z, Scatolin GN, Wang X, Yau K, Tao L, Tong X, Wang S, Shi K-X, Evseenko D, Handel BV, Zhang B, Wang Y, Iyyappan R, Ojeda-Rojas OA, Hu G, McGinnis L, Paulson R, Mckim D, Kong X, Xia X, Zhang J, Chen YE, Xu J, Jiang Z, Ying Q-L. A universal 6iL/E4 culture system for deriving and maintaining embryonic stem cells across mammalian species. bioRxiv. 2025;2025.2005.2020.654948. PMid:40475639.
Wang Y, Ming H, Yu L, Li J, Zhu L, Sun HX, Pinzon-Arteaga CA, Wu J, Jiang Z. Establishment of bovine trophoblast stem cells. Cell Rep. 2023;42(5):112439.
Weeratunga P, Harman RM, Van de Walle GR. Induced pluripotent stem cells from domesticated ruminants and their potential for enhancing livestock production. Front Vet Sci. 2023;10:1129287.
Yu L, Wei Y, Duan J, Schmitz DA, Sakurai M, Wang L, Wang K, Zhao S, Hon GC, Wu J. Blastocyst-like structures generated from human pluripotent stem cells. Nature. 2021a;591(7851):620-6.
Yu L, Wei Y, Sun HX, Mahdi AK, Pinzon Arteaga CA, Sakurai M, Schmitz DA, Zheng C, Ballard ED, Li J, Tanaka N, Kohara A, Okamura D, Mutto AA, Gu Y, Ross PJ, Wu J. Derivation of intermediate pluripotent stem cells amenable to primordial germ cell specification. Cell Stem Cell. 2021b;28(3):550-567.e12.
Zhang J, Li H, Li L, Wu J, Song L, Liu X, Pan Z, Zhou C, Li W, Liu Z, Jiao M, Hu M, Dong Z, Zhang H, Shi B, Wang Y, Wang D, Carter B, Zhao S, Ren G, Zhao Y, Zhang Y. Super RNA Pol II domains enhance minor ZGA through 3D interaction to ensure the integrity of major transcriptional waves in late-ZGA mammals. Cell Genom. 2025;5(6):100856.
Zhao BS, Wang X, Beadell AV, Lu Z, Shi H, Kuuspalu A, Ho RK, He C. m(6)A-dependent maternal mRNA clearance facilitates zebrafish maternal-to-zygotic transition. Nature. 2017;542(7642):475-8.
Zhao L, Gao X, Zheng Y, Wang Z, Zhao G, Ren J, Zhang J, Wu J, Wu B, Chen Y, Sun W, Li Y, Su J, Ding Y, Gao Y, Liu M, Bai X, Sun L, Cao G, Tang F, Bao S, Liu P, Li X. Establishment of bovine expanded potential stem cells. Proc Natl Acad Sci USA. 2021;118(15):e2018505118.
Zhou C, Halstead MM, Bonnet-Garnier A, Schultz RM, Ross PJ. Histone remodeling reflects conserved mechanisms of bovine and human preimplantation development. EMBO Rep. 2023;24(3):e55726.
Zhu M, Zernicka-Goetz M. Principles of self-organization of the mammalian embryo. Cell. 2020;183(6):1467-78.
Zhu L, Marjani SL, Jiang Z. The epigenetics of gametes and early embryos and potential long-range consequences in livestock species-filling in the picture with epigenomic analyses. Front Genet. 2021;12:557934.
Zhu L, Zhou T, Iyyappan R, Ming H, Dvoran M, Wang Y, Chen Q, Roberts RM, Susor A, Jiang Z. High-resolution ribosome profiling reveals translational selectivity for transcripts in bovine preimplantation embryo development. Development. 2022;149(21):dev200819.
Zhu L, Ming H, Scatolin GN, Xiao A, Jiang Z. METTL7A improves bovine IVF embryo competence by attenuating oxidative stressdagger. Biol Reprod. 2025;112(4):628-39.
Submitted date:
05/06/2025
Accepted date:
07/19/2025
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