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Annual Review of Animal Biosciences

Volume 13, 2025

Ruminating on Bovine Implantation: Its Importance in Fertility, Food Production, Conservation, and Health

Abstract

Implantation in cattle is a key developmental checkpoint for pregnancy success. It involves careful spatiotemporal changes to the transcriptional landscape of the endometrium, with the heterogeneous nature of the endometrium increasing the complexity of understanding of the mechanism involved. Implantation is impacted by the developmental competency of the embryo, use of assisted reproductive technologies, and the environment in which this process occurs. We identify the factors that most impact the implantation process in cattle and highlight how it differs with that in other placental mammals. We propose the major areas that lack evidence are the mechanism(s) by which implantation itself occurs and how different stressors alter this process. Our understanding is hindered by a lack of appropriate in vitro models; however, development of novel 3D tools and available data sets will further elucidate the implantation process. Perhaps more importantly, this will develop methods to mitigate against these stressors to improve implantation success and offspring health.

Keyword(s): conceptus, embryo, endometrium, mammalian implantation, receptivity, uterus
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2025-02-18
2025-06-19
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Literature Cited

  1. 1.
    Tinning H, Edge JC, DeBem THC, Deligianni F, Giovanardi G, et al. 2023.. Review: endometrial function in pregnancy establishment in cattle. . Animal 17:(Suppl. 1):100751
     [Crossref] [Google Scholar]
  2. 2.
    Brooks K, Burns G, Spencer TE. 2014.. Conceptus elongation in ruminants: roles of progesterone, prostaglandin, interferon tau and cortisol. . J. Anim. Sci. Biotechnol. 5::53
     [Crossref] [Google Scholar]
  3. 3.
    Forde N, Beltman ME, Lonergan P, Diskin M, Roche JF, Crowe MA. 2011.. Oestrous cycles in Bos taurus cattle. . Anim. Reprod. Sci. 124:(3):163–69
     [Crossref] [Google Scholar]
  4. 4.
    Chenault JR, Thatcher WW, Kalra PS, Abrams RM, Wilcox CJ. 1975.. Transitory changes in plasma progestins, estradiol, and luteinizing hormone approaching ovulation in the bovine. . J. Dairy Sci. 58:(5):709–17
     [Crossref] [Google Scholar]
  5. 5.
    Davoodi S, Cooke RF, Fernandes ACC, Cappellozza BI, Vasconcelos JLM, Cerri RLA. 2016.. Expression of estrus modifies the gene expression profile in reproductive tissues on Day 19 of gestation in beef cows. . Theriogenology 85:(4):645–55
     [Crossref] [Google Scholar]
  6. 6.
    Bazer FW, Spencer TE, Johnson GA, Burghardt RC. 2011.. Uterine receptivity to implantation of blastocysts in mammals. . Front. Biosci. 3:(2):745–67
     [Crossref] [Google Scholar]
  7. 7.
    Binelli M, Silva FACC, Rocha CC, Martins T, Sponchiado M, et al. 2022.. Endometrial receptivity in cattle: the mutual reprogramming paradigm. . Anim. Reprod. 19:(4):e20220097
     [Crossref] [Google Scholar]
  8. 8.
    Okumu LA, Forde N, Fahey AG, Fitzpatrick E, Roche JF, et al. 2010.. The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. . Reproduction 140:(1):143–53
     [Crossref] [Google Scholar]
  9. 9.
    Carter F, Forde N, Duffy P, Wade M, Fair T, et al. 2008.. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. . Reprod. Fertil. Dev. 20:(3):368–75
     [Crossref] [Google Scholar]
  10. 10.
    Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, et al. 2009.. Progesterone and conceptus elongation in cattle: A direct effect on the embryo or an indirect effect via the endometrium?. Reproduction 138:(3):507–17
     [Crossref] [Google Scholar]
  11. 11.
    Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D. 1980.. Collection, description and transfer of embryos from cattle 10–16 days after oestrus. . J. Reprod. Fertil. 59:(1):205–16
     [Crossref] [Google Scholar]
  12. 12.
    Robinson RS, Fray MD, Wathes DC, Lamming GE, Mann GE. 2006.. In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow. . Mol. Reprod. Dev. 73:(4):470–74
     [Crossref] [Google Scholar]
  13. 13.
    Forde N, Carter F, Fair T, Crowe MA, Evans ACO, et al. 2009.. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. . Biol. Reprod. 81:(4):784–94
     [Crossref] [Google Scholar]
  14. 14.
    Alfattah MA, Correia CN, Browne JA, McGettigan PA, Pluta K, et al. 2024.. Transcriptomics analysis of the bovine endometrium during the perioestrus period. . PLOS ONE 19:(3):e0301005
     [Crossref] [Google Scholar]
  15. 15.
    Pereira G, Guo Y, Silva E, Bevilacqua C, Charpigny G, et al. 2022.. Progesterone differentially affects the transcriptomic profiles of cow endometrial cell types. . BMC Genom. 23:(1):82
     [Crossref] [Google Scholar]
  16. 16.
    Simintiras CA, Sánchez JM, McDonald M, Lonergan P. 2019.. The influence of progesterone on bovine uterine fluid energy, nucleotide, vitamin, cofactor, peptide, and xenobiotic composition during the conceptus elongation-initiation window. . Sci. Rep. 9:(1):7716
     [Crossref] [Google Scholar]
  17. 17.
    Martins T, Pugliesi G, Sponchiado M, Gonella-Diaza AM, Ojeda-Rojas OA, et al. 2018.. Perturbations in the uterine luminal fluid composition are detrimental to pregnancy establishment in cattle. . J. Anim. Sci. Biotechnol. 9::70
     [Crossref] [Google Scholar]
  18. 18.
    Bazer FW, Spencer TE, Ott TL. 1997.. Interferon tau: a novel pregnancy recognition signal. . Am. J. Reprod. Immunol. 37:(6):412–20
     [Crossref] [Google Scholar]
  19. 19.
    Spencer TE, Becker WC, George P, Mirando MA, Ogle TF, Bazer FW. 1995.. Ovine interferon-tau inhibits estrogen receptor up-regulation and estrogen-induced luteolysis in cyclic ewes. . Endocrinology 136:(11):4932–44
     [Crossref] [Google Scholar]
  20. 20.
    Spencer TE, Ing NH, Ott TL, Mayes JS, Becker WC, et al. 1995.. Intrauterine injection of ovine interferon-tau alters oestrogen receptor and oxytocin receptor expression in the endometrium of cyclic ewes. . J. Mol. Endocrinol. 15:(2):203–20
     [Crossref] [Google Scholar]
  21. 21.
    Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, et al. 2009.. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. . Physiol. Genom. 39:(1):14–27
     [Crossref] [Google Scholar]
  22. 22.
    Pedersen HS, Mazzoni G, Stroebech L, Kadarmideen H, Hyttel P, Callesen H. 2017.. Basic and practical aspects of pregnancy establishment in cattle. . Anim. Reprod. 14::581–88
     [Crossref] [Google Scholar]
  23. 23.
    Bazer FW, Thatcher WW. 2017.. Chronicling the discovery of interferon tau. . Reproduction 154:(5):F11–20
     [Crossref] [Google Scholar]
  24. 24.
    Bazer FW, Ying W, Wang X, Dunlap KA, Zhou B, et al. 2015.. The many faces of interferon tau. . Amino Acids 47:(3):449–60
     [Crossref] [Google Scholar]
  25. 25.
    Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. 1998.. How cells respond to interferons. . Annu. Rev. Biochem. 67::227–64
     [Crossref] [Google Scholar]
  26. 26.
    Austin KJ, Carr AL, Pru JK, Hearne CE, George EL, et al. 2004.. Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy. . Endocrinology 145:(2):967–75
     [Crossref] [Google Scholar]
  27. 27.
    Sakumoto R, Hayashi K-G, Fujii S, Kanahara H, Hosoe M, et al. 2017.. Possible roles of CC- and CXC-chemokines in regulating bovine endometrial function during early pregnancy. . Int. J. Mol. Sci. 18:(4):742
     [Crossref] [Google Scholar]
  28. 28.
    Nagaoka K, Nojima H, Watanabe F, Chang K-T, Christenson RK, et al. 2003.. Regulation of blastocyst migration, apposition, and initial adhesion by a chemokine, interferon γ-inducible protein 10 kDa (IP-10), during early gestation. . J. Biol. Chem. 278:(31):29048–56
     [Crossref] [Google Scholar]
  29. 29.
    Hansen TR, Sinedino LDP, Spencer TE. 2017.. Paracrine and endocrine actions of interferon tau (IFNT). . Reproduction 154:(5):F45–59
     [Crossref] [Google Scholar]
  30. 30.
    Spencer TE, Forde N, Lonergan P. 2016.. The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. . J. Dairy Sci. 99:(7):5941–50
     [Crossref] [Google Scholar]
  31. 31.
    Mathew DJ, Sánchez JM, Passaro C, Charpigny G, Behura SK, et al. 2019.. Interferon tau-dependent and independent effects of the bovine conceptus on the endometrial transcriptome. . Biol. Reprod. 100:(2):365–80
     [Crossref] [Google Scholar]
  32. 32.
    Bauersachs S, Ulbrich SE, Reichenbach H-D, Reichenbach M, Büttner M, et al. 2012.. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. . Biol. Reprod. 86:(2):46
     [Crossref] [Google Scholar]
  33. 33.
    Forde N, Bazer FW, Spencer TE, Lonergan P. 2015.. ‘Conceptualizing’ the endometrium: identification of conceptus-derived proteins during early pregnancy in cattle. . Biol. Reprod. 92:(6):156
     [Crossref] [Google Scholar]
  34. 34.
    Malo Estepa I, Tinning H, Rosas Vasconcelos EJ, Fernandez-Fuertes B, Sánchez JM, et al. 2020.. Protein synthesis by day 16 bovine conceptuses during the time of maternal recognition of pregnancy. . Int. J. Mol. Sci. 21:(8):2870
     [Crossref] [Google Scholar]
  35. 35.
    Tinning H, Taylor A, Wang D, Constantinides B, Sutton R, et al. 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?. FASEB J. 34:(8):11015–29
     [Crossref] [Google Scholar]
  36. 36.
    Burns GW, Brooks KE, Spencer TE. 2016.. Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. . Biol. Reprod. 94:(3):56
     [Crossref] [Google Scholar]
  37. 37.
    De Bem THC, Bridi A, Tinning H, Sampaio RV, Malo-Estepa I, et al. 2023.. Biosensor capability of the endometrium is mediated in part, by altered miRNA cargo from conceptus-derived extracellular vesicles. . FASEB J. 38:(10):e23639
     [Crossref] [Google Scholar]
  38. 38.
    Imakawa K, Matsuno Y, Fujiwara H. 2022.. New roles for EVs, miRNA and lncRNA in bovine embryo implantation. . Front. Vet. Sci. 9::944370
     [Crossref] [Google Scholar]
  39. 39.
    Miller DJ. 2024.. Sperm in the mammalian female reproductive tract: surfing through the tract to try to beat the odds. . Annu. Rev. Anim. Biosci. 12::301–19
     [Crossref] [Google Scholar]
  40. 40.
    Schjenken JE, Robertson SA. 2020.. The female response to seminal fluid. . Physiol. Rev. 100:(3):1077–117
     [Crossref] [Google Scholar]
  41. 41.
    Paiva L, Silva M, Carrasco R, Ratto V, Goicochea J, Ratto M. 2022.. Seminal plasma nerve growth factor signaling on the reproductive physiology of female llamas. . Anim. Reprod. 19:(4):e20220116
     [Crossref] [Google Scholar]
  42. 42.
    Bromfield JJ. 2016.. A role for seminal plasma in modulating pregnancy outcomes in domestic species. . Reproduction 152:(6):R223–32
     [Crossref] [Google Scholar]
  43. 43.
    Howe GR, Black DL. 1963.. Spermatozoan transport and leucocytic responses in the reproductive tract of calves. . J. Reprod. Fertil. 6::305–11
     [Crossref] [Google Scholar]
  44. 44.
    Shen Q, Wu X, Chen J, He C, Wang Z, et al. 2023.. Immune regulation of seminal plasma on the endometrial microenvironment: physiological and pathological conditions. . Int. J. Mol. Sci. 24:(19):14639
     [Crossref] [Google Scholar]
  45. 45.
    Sharkey DJ, Glynn DJ, Schjenken JE, Tremellen KP, Robertson SA. 2018.. Interferon-gamma inhibits seminal plasma induction of colony-stimulating factor 2 in mouse and human reproductive tract epithelial cells. . Biol. Reprod. 99:(3):514–26
     [Crossref] [Google Scholar]
  46. 46.
    Woodward EM, Christoffersen M, Campos J, Betancourt A, Horohov D, et al. 2013.. Endometrial inflammatory markers of the early immune response in mares susceptible or resistant to persistent breeding-induced endometritis. . Reproduction 145:(3):289–96
     [Crossref] [Google Scholar]
  47. 47.
    O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. 2004.. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. . Reproduction 128:(2):237–47
     [Crossref] [Google Scholar]
  48. 48.
    Svensson A, Jiwakanon J, Fossum C, Dalin A-M. 2021.. Expression of IL-23 in gilt endometrium and oviduct after insemination with seminal plasma, spermatozoa or semen extender. . BMC Res. Notes 14:(1):221
     [Crossref] [Google Scholar]
  49. 49.
    Scott JL, Ketheesan N, Summers PM. 2009.. Spermatozoa and seminal plasma induce a greater inflammatory response in the ovine uterus at oestrus than dioestrus. . Reprod. Fertil. Dev. 21:(7):817–26
     [Crossref] [Google Scholar]
  50. 50.
    Ibrahim LA, Rizo JA, Fontes PLP, Lamb GC, Bromfield JJ. 2019.. Seminal plasma modulates expression of endometrial inflammatory meditators in the bovine. . Biol. Reprod. 100:(3):660–71
     [Crossref] [Google Scholar]
  51. 51.
    Nongbua T, Guo Y, Ntallaris T, Rubér M, Rodriguez-Martinez H, et al. 2020.. Bull seminal plasma stimulates in vitro production of TGF-β, IL-6 and IL-8 from bovine endometrial epithelial cells, depending on dose and bull fertility. . J. Reprod. Immunol. 142::103179
     [Crossref] [Google Scholar]
  52. 52.
    Sharkey DJ, Macpherson AM, Tremellen KP, Mottershead DG, Gilchrist RB, Robertson SA. 2012.. TGF-β mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. . J. Immunol. 189:(2):1024–35
     [Crossref] [Google Scholar]
  53. 53.
    Bai R, Latifi Z, Kusama K, Nakamura K, Shimada M, Imakawa K. 2018.. Induction of immune-related gene expression by seminal exosomes in the porcine endometrium. . Biochem. Biophys. Res. Commun. 495:(1):1094–101
     [Crossref] [Google Scholar]
  54. 54.
    Stewart JL, Mercadante VRG, Dias NW, Canisso IF, Yau P, et al. 2018.. Nerve growth factor-beta, purified from bull seminal plasma, enhances corpus luteum formation and conceptus development in Bos taurus cows. . Theriogenology 106::30–38
     [Crossref] [Google Scholar]
  55. 55.
    Ortiz WG, Rizo JA, Carvalheira LR, Ahmed BMS, Estrada-Cortes E, et al. 2019.. Effects of intrauterine infusion of seminal plasma at artificial insemination on fertility of lactating Holstein cows. . J. Dairy Sci. 102:(7):6587–94
     [Crossref] [Google Scholar]
  56. 56.
    Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. 2014.. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. . PNAS 111:(6):2200–5
     [Crossref] [Google Scholar]
  57. 57.
    Wong CL, Chan OC, Lee KH, O WS, Chow PH. 2008.. Absence of paternal accessory sex glands dysregulates preimplantation embryo cell cycle and causes early oviductal-uterine transit in the golden hamster in vivo. . Fertil. Steril. 89:(4):1021–24
     [Crossref] [Google Scholar]
  58. 58.
    Yang C, Zeng Q-X, Liu J-C, Yeung WS-B, Zhang JV, Duan Y-G. 2023.. Role of small RNAs harbored by sperm in embryonic development and offspring phenotype. . Andrology 11:(4):770–82
     [Crossref] [Google Scholar]
  59. 59.
    Alghamdi AS, Lovaas BJ, Bird SL, Lamb GC, Rendahl AK, et al. 2009.. Species-specific interaction of seminal plasma on sperm-neutrophil binding. . Anim. Reprod. Sci. 114:(4):331–44
     [Crossref] [Google Scholar]
  60. 60.
    Donnellan EM, Cormican P, Reid C, Duggan G, Stiavnicka M, et al. 2023.. The transcriptomic response of bovine uterine tissue is altered in response to sperm from high- and low-fertility bulls. . Biol. Reprod. 108:(6):912–21
     [Crossref] [Google Scholar]
  61. 61.
    Recuero S, Sánchez JM, Mateo-Otero Y, Bagés-Arnal S, McDonald M, et al. 2020.. Mating to intact, but not vasectomized, males elicits changes in the endometrial transcriptome: insights from the bovine model. . Front. Cell Dev. Biol. 8::547
     [Crossref] [Google Scholar]
  62. 62.
    Mateo-Otero Y, Sánchez JM, Recuero S, Bagés-Arnal S, McDonald M, et al. 2020.. Effect of exposure to seminal plasma through natural mating in cattle on conceptus length and gene expression. . Front. Cell Dev. Biol. 8::341
     [Crossref] [Google Scholar]
  63. 63.
    Odhiambo JF, Poole DH, Hughes L, Dejarnette JM, Inskeep EK, Dailey RA. 2009.. Pregnancy outcome in dairy and beef cattle after artificial insemination and treatment with seminal plasma or transforming growth factor beta-1. . Theriogenology 72:(4):566–71
     [Crossref] [Google Scholar]
  64. 64.
    Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. 2009.. Comparative aspects of implantation. . Reproduction 138:(2):195–209
     [Crossref] [Google Scholar]
  65. 65.
    Stenhouse C, Seo H, Wu G, Johnson GA, Bazer FW. 2022.. Insights into the regulation of implantation and placentation in humans, rodents, sheep, and pigs. . Adv. Exp. Med. Biol. 1354::25–48
     [Crossref] [Google Scholar]
  66. 66.
    Paulson EE, Comizzoli P. 2021.. Endometrial receptivity and embryo implantation in carnivores-commonalities and differences with other mammalian species. . Biol. Reprod. 104:(4):771–83
     [Crossref] [Google Scholar]
  67. 67.
    Chavan AR, Griffith OW, Stadtmauer DJ, Maziarz J, Pavlicev M, et al. 2021.. Evolution of embryo implantation was enabled by the origin of decidual stromal cells in eutherian mammals. . Mol. Biol. Evol. 38:(3):1060–74
     [Crossref] [Google Scholar]
  68. 68.
    McGowen MR, Erez O, Romero R, Wildman DE. 2014.. The evolution of embryo implantation. . Int. J. Dev. Biol. 58:(2–4):155–61
     [Crossref] [Google Scholar]
  69. 69.
    Malkowska A, Penfold C, Bergmann S, Boroviak TE. 2022.. A hexa-species transcriptome atlas of mammalian embryogenesis delineates metabolic regulation across three different implantation modes. . Nat. Commun. 13::3407
     [Crossref] [Google Scholar]
  70. 70.
    Wooding FBP. 2022.. The ruminant placental trophoblast binucleate cell: an evolutionary breakthrough. . Biol. Reprod. 107:(3):705–16
     [Crossref] [Google Scholar]
  71. 71.
    Klisch K, Schraner EM. 2020.. Intraluminal vesicles of binucleate trophoblast cell granules are a possible source of placental exosomes in ruminants. . Placenta 90::58–61
     [Crossref] [Google Scholar]
  72. 72.
    Carter AM. 2020.. Evolution of placentation in cattle and antelopes. . Anim. Reprod. 16:(1):3–17
     [Crossref] [Google Scholar]
  73. 73.
    Attiger J, Boos A, Klisch K. 2018.. Morphological characterization of basally located uninucleate trophoblast cells as precursors of bovine binucleate trophoblast giant cells. . Cells Tissues Organs 205:(3):151–63
     [Crossref] [Google Scholar]
  74. 74.
    Wiltbank MC, Monteiro PLJ, Domingues RR, Andrade JPN, Mezera MA. 2023.. Review: maintenance of the ruminant corpus luteum during pregnancy: interferon-tau and beyond. . Animal 17:(Suppl. 1):100827
     [Crossref] [Google Scholar]
  75. 75.
    Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PLJ, et al. 2016.. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. . Theriogenology 86:(1):239–53
     [Crossref] [Google Scholar]
  76. 76.
    Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, et al. 2009.. The endometrium responds differently to cloned versus fertilized embryos. . PNAS 106:(14):5681–86
     [Crossref] [Google Scholar]
  77. 77.
    Macklon NS, Brosens JJ. 2014.. The human endometrium as a sensor of embryo quality. . Biol. Reprod. 91:(4):98
     [Crossref] [Google Scholar]
  78. 78.
    Nakamura K, Kusama K, Ideta A, Imakawa K, Hori M. 2020.. IFNT-independent effects of intrauterine extracellular vesicles (EVs) in cattle. . Reproduction 159:(5):503–11
     [Crossref] [Google Scholar]
  79. 79.
    Nakamura K, Kusama K, Hori M, Imakawa K. 2023.. Global analyses and potential effects of extracellular vesicles on the establishment of conceptus implantation during the peri-implantation period. . J. Reprod. Dev. 69:(5):246–53
     [Crossref] [Google Scholar]
  80. 80.
    Collier RJ, Dahl GE, VanBaale MJ. 2006.. Major advances associated with environmental effects on dairy cattle. . J. Dairy Sci. 89:(4):1244–53
     [Crossref] [Google Scholar]
  81. 81.
    Roth Z. 2017.. Effect of heat stress on reproduction in dairy cows: insights into the cellular and molecular responses of the oocyte. . Annu. Rev. Anim. Biosci. 5::151–70
     [Crossref] [Google Scholar]
  82. 82.
    Shahat AM, Rizzoto G, Kastelic JP. 2020.. Amelioration of heat stress-induced damage to testes and sperm quality. . Theriogenology 158::84–96
     [Crossref] [Google Scholar]
  83. 83.
    Hamilton TRDS, Mendes CM, de Castro LS, de Assis PM, Siqueira AFP, et al. 2016.. Evaluation of lasting effects of heat stress on sperm profile and oxidative status of ram semen and epididymal sperm. . Oxid. Med. Cell Longev. 2016.:1687657
     [Google Scholar]
  84. 84.
    Diniz WJS, Ward AK, McCarthy KL, Kassetas CJ, Baumgaertner F, et al. 2023.. Periconceptual maternal nutrition affects fetal liver programming of energy- and lipid-related genes. . Animals 13:(4):600
     [Crossref] [Google Scholar]
  85. 85.
    Thundathil JC, Dance AL, Kastelic JP. 2016.. Fertility management of bulls to improve beef cattle productivity. . Theriogenology 86:(1):397–405
     [Crossref] [Google Scholar]
  86. 86.
    Mansouri A, Yousef MS, Kowsar R, Usui N, Akthar I, Miyamoto A. 2023.. Sperm activate TLR2/TLR1 heterodimerization to induce a weak proinflammatory response in the bovine uterus. . Front. Immunol. 14::1158090
     [Crossref] [Google Scholar]
  87. 87.
    Diemer J, Hahn J, Goldenbogen B, Müller K, Klipp E. 2021.. Sperm migration in the genital tract—in silico experiments identify key factors for reproductive success. . PLOS Comput. Biol. 17:(7):e1009109
     [Crossref] [Google Scholar]
  88. 88.
    Gaughan JB, Bonner SL, Loxton I, Mader TL. 2013.. Effects of chronic heat stress on plasma concentration of secreted heat shock protein 70 in growing feedlot cattle. . J. Anim. Sci. 91:(1):120–29
     [Crossref] [Google Scholar]
  89. 89.
    Adur MK, Seibert JT, Romoser MR, Bidne KL, Baumgard LH, et al. 2022.. Porcine endometrial heat shock proteins are differentially influenced by pregnancy status, heat stress, and altrenogest supplementation during the peri-implantation period. . J. Anim. Sci. 100:(7):skac129
     [Crossref] [Google Scholar]
  90. 90.
    Vasconcelos JLM, Demétrio DGB, Santos RM, Chiari JR, Rodrigues CA, Sá Filho OG. 2006.. Factors potentially affecting fertility of lactating dairy cow recipients. . Theriogenology 65:(1):192–200
     [Crossref] [Google Scholar]
  91. 91.
    Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank MC. 2002.. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. . J. Dairy Sci. 85:(11):2803–12
     [Crossref] [Google Scholar]
  92. 92.
    Rizos D, Carter F, Besenfelder U, Havlicek V, Lonergan P. 2010.. Contribution of the female reproductive tract to low fertility in postpartum lactating dairy cows. . J. Dairy Sci. 93:(3):1022–29
     [Crossref] [Google Scholar]
  93. 93.
    Monteiro APA, Tao S, Thompson IMT, Dahl GE. 2016.. In utero heat stress decreases calf survival and performance through the first lactation. . J. Dairy Sci. 99:(10):8443–50
     [Crossref] [Google Scholar]
  94. 94.
    Lewis K, Carter LS, Bradley A, Dewhurst R, Forde N, et al. 2024.. Quantification of the effect of in-utero events on lifetime resilience in dairy cows. . J. Dairy Sci. 107:(7):4616–33
     [Crossref] [Google Scholar]
  95. 95.
    Kasimanickam R, Kasimanickam V. 2021.. Impact of heat stress on embryonic development during first 16 days of gestation in dairy cows. . Sci. Rep. 11::14839
     [Crossref] [Google Scholar]
  96. 96.
    Skibiel AL, Dado-Senn B, Fabris TF, Dahl GE, Laporta J. 2018.. In utero exposure to thermal stress has long-term effects on mammary gland microstructure and function in dairy cattle. . PLOS ONE 13:(10):e0206046
     [Crossref] [Google Scholar]
  97. 97.
    Sales JNS, Iguma LT, Batista RITP, Quintão CCR, Gama MAS, et al. 2015.. Effects of a high-energy diet on oocyte quality and in vitro embryo production in Bos indicus and Bos taurus cows. . J. Dairy Sci. 98:(5):3086–99
     [Crossref] [Google Scholar]
  98. 98.
    Ferreira RM, Ayres H, Chiaratti MR, Ferraz ML, Araújo AB, et al. 2011.. The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. . J. Dairy Sci. 94:(5):2383–92
     [Crossref] [Google Scholar]
  99. 99.
    Sakumoto R, Hayashi K-G, Saito S, Kanahara H, Kizaki K, Iga K. 2015.. Comparison of the global gene expression profiles in the bovine endometrium between summer and autumn. . J. Reprod. Dev. 61:(4):297–303
     [Crossref] [Google Scholar]
  100. 100.
    Kawano K, Yanagawa Y, Nagano M, Katagiri S. 2022.. Effects of heat stress on the endometrial epidermal growth factor profile and fertility in dairy cows. . J. Reprod. Dev. 68:(2):144–51
     [Crossref] [Google Scholar]
  101. 101.
    Sakai S, Yagi M, Fujime N, Kuse M, Sakumoto R, et al. 2021.. Heat stress influences the attenuation of prostaglandin synthesis by interferon tau in bovine endometrial cells. . Theriogenology 165::52–58
     [Crossref] [Google Scholar]
  102. 102.
    Sakai S, Hatabu T, Yamamoto Y, Kimura K. 2020.. Alteration of chemokine production in bovine endometrial epithelial and stromal cells under heat stress conditions. . Physiol Rep. 8:(22):e14640
     [Crossref] [Google Scholar]
  103. 103.
    Leroy JLMR, Van Soom A, Opsomer G, Bols PEJ. 2008.. The consequences of metabolic changes in high-yielding dairy cows on oocyte and embryo quality. . Animal 2:(8):1120–27
     [Crossref] [Google Scholar]
  104. 104.
    Bauersachs S, Simintiras CA, Sturmey RG, Krebs S, Bick J, et al. 2017.. Effect of metabolic status on conceptus-maternal interactions on day 19 in dairy cattle: II. Effects on the endometrial transcriptome. . Biol. Reprod. 97:(3):413–25
     [Crossref] [Google Scholar]
  105. 105.
    Forde N, Simintiras CA, Sturmey RG, Graf A, Wolf E, et al. 2017.. Effect of lactation on conceptus-maternal interactions at the initiation of implantation in cattle: I. Effects on the conceptus transcriptome and amino acid composition of the uterine luminal fluid. . Biol. Reprod. 97:(6):798–809
     [Crossref] [Google Scholar]
  106. 106.
    Moraes JGN, Behura SK, Geary TW, Spencer TE. 2020.. Analysis of the uterine lumen in fertility-classified heifers: I. Glucose, prostaglandins, and lipids. . Biol. Reprod. 102:(2):456–74
     [Crossref] [Google Scholar]
  107. 107.
    Caton JS, Crouse MS, Reynolds LP, Neville TL, Dahlen CR, et al. 2019.. Maternal nutrition and programming of offspring energy requirements. . Transl. Anim. Sci. 3:(3):976–90
     [Crossref] [Google Scholar]
  108. 108.
    Martin JL, Vonnahme KA, Adams DC, Lardy GP, Funston RN. 2007.. Effects of dam nutrition on growth and reproductive performance of heifer calves. . J. Anim. Sci. 85:(3):841–47
     [Crossref] [Google Scholar]
  109. 109.
    Adamiak SJ, Mackie K, Watt RG, Webb R, Sinclair KD. 2005.. Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle. . Biol. Reprod. 73:(5):918–26
     [Crossref] [Google Scholar]
  110. 110.
    Sarlo Davila KM, Hamblen H, Hansen PJ, Dikmen S, Oltenacu PA, Mateescu RG. 2019.. Genetic parameters for hair characteristics and core body temperature in a multibreed Brahman-Angus herd. . J. Anim. Sci. 97:(8):3246–52
     [Crossref] [Google Scholar]
  111. 111.
    Hansen PJ. 2020.. Prospects for gene introgression or gene editing as a strategy for reduction of the impact of heat stress on production and reproduction in cattle. . Theriogenology 154::190–202
     [Crossref] [Google Scholar]
  112. 112.
    Carmickle AT, Larson CC, Hernandez FS, Pereira JMV, Ferreira FC, et al. 2022.. Physiological responses of Holstein calves and heifers carrying the SLICK1 allele to heat stress in California and Florida dairy farms. . J. Dairy Sci. 105:(11):9216–25
     [Crossref] [Google Scholar]
  113. 113.
    Macias Franco A, Elins Moreira da Silva A, Holton G, Brody T, Alves Fonseca M. 2024.. Establishing the relationship between wildfire smoke and performance metrics on finished beef cattle in Western Rangelands. . Transl. Anim. Sci. 8::txae022
     [Crossref] [Google Scholar]
  114. 114.
    Wrobel MH, Mlynarczuk J. 2020.. The effect of polychlorinated biphenyls (PCBs) on bovine oviductal contractions and LIF synthesis during estrous cycle, in vitro studies. . Res. Vet. Sci. 133::188–93
     [Crossref] [Google Scholar]
  115. 115.
    Wrobel MH, Mlynarczuk J, Kotwica J. 2010.. Influence of polychlorinated biphenyls and their hydroxylated metabolites on prostaglandins secretion from epithelial cells of bovine oviduct, in vitro. . Toxicology 270:(2–3):85–91
     [Crossref] [Google Scholar]
  116. 116.
    Hallberg I, Persson S, Olovsson M, Moberg M, Ranefall P, et al. 2022.. Bovine oocyte exposure to perfluorohexane sulfonate (PFHxS) induces phenotypic, transcriptomic, and DNA methylation changes in resulting embryos in vitro. . Reprod. Toxicol. 109::19–30
     [Crossref] [Google Scholar]
  117. 117.
    Ripple WJ, Newsome TM, Wolf C, Dirzo R, Everatt KT, et al. 2015.. Collapse of the world's largest herbivores. . Sci. Adv. 1:(4):e1400103
     [Crossref] [Google Scholar]
  118. 118.
    Berger J, Buuveibaatar B, Mishra C. 2013.. Globalization of the cashmere market and the decline of large mammals in central Asia. . Conserv. Biol. 27:(4):679–89
     [Crossref] [Google Scholar]
  119. 119.
    Di Marco M, Collen B, Rondinini C, Mace GM. 2015.. Historical drivers of extinction risk: using past evidence to direct future monitoring. . Proc. Biol. Sci. 282:( 1813.):20150928
     [Google Scholar]
  120. 120.
    Lees CM, Wilcken J. 2009.. Sustaining the Ark: the challenges faced by zoos in maintaining viable populations. . Int. Zoo Yearb. 43:(1):6–18
     [Crossref] [Google Scholar]
  121. 121.
    Pukazhenthi BS. 2016.. Saving wild ungulate diversity through enhanced management and sperm cryopreservation. . Reprod. Fertil. Dev. 28:(8):1133–44
     [Crossref] [Google Scholar]
  122. 122.
    Holt WV, Comizzoli P. 2022.. Opportunities and limitations for reproductive science in species conservation. . Annu. Rev. Anim. Biosci. 10::491–511
     [Crossref] [Google Scholar]
  123. 123.
    Roth TL, Swanson WF. 2018.. From petri dishes to politics—a multi-pronged approach is essential for saving endangered species. . Nat. Commun. 9::2588
     [Crossref] [Google Scholar]
  124. 124.
    Cowl VB, Comizzoli P, Appeltant R, Bolton RL, Browne RK, et al. 2024.. Cloning for the twenty-first century and its place in endangered species conservation. . Annu. Rev. Anim. Biosci. 12::91–112
     [Crossref] [Google Scholar]
  125. 125.
    Swegen A, Appeltant R, Williams SA. 2023.. Cloning in action: Can embryo splitting, induced pluripotency and somatic cell nuclear transfer contribute to endangered species conservation?. Biol. Rev. Camb. Philos. Soc. 98:(4):1225–49
     [Crossref] [Google Scholar]
  126. 126.
    Borges AA, Pereira AF. 2019.. Potential role of intraspecific and interspecific cloning in the conservation of wild mammals. . Zygote 27:(3):111–17
     [Crossref] [Google Scholar]
  127. 127.
    Le Gac S, Ferraz M, Venzac B, Comizzoli P. 2021.. Understanding and assisting reproduction in wildlife species using microfluidics. . Trends Biotechnol. 39:(6):584–97
     [Crossref] [Google Scholar]
  128. 128.
    Paulson RJ, Comizzoli P. 2018.. Addressing challenges in developing and implementing successful in vitro fertilization in endangered species: an opportunity for humanity to “give back. .” Fertil. Steril. 109:(3):418–19
     [Crossref] [Google Scholar]
  129. 129.
    Comizzoli P. 2021.. Adding new ingredients to the recipe for successful embryo transfers. . J. Assist. Reprod. Genet. 38:(5):1019–20
     [Crossref] [Google Scholar]
  130. 130.
    Patton ML, Jöchle W, Penfold LM. 2007.. Review of contraception in ungulate species. . Zoo Biol. 26:(4):311–26
     [Crossref] [Google Scholar]
  131. 131.
    Sontakke SD. 2018.. Monitoring and controlling ovarian activities in wild ungulates. . Theriogenology 109::31–41
     [Crossref] [Google Scholar]
  132. 132.
    da Silva AM, Pereira AF, Comizzoli P, Silva AR. 2020.. Cryopreservation and culture of testicular tissues: an essential tool for biodiversity preservation. . Biopreserv. Biobank. 18:(3):235–43
     [Crossref] [Google Scholar]
  133. 133.
    Campos LB, Praxedes ÉCG, Saraiva MVA, Comizzoli P, Silva AR. 2019.. Advances and challenges of using ovarian preantral follicles to develop biobanks of wild mammals. . Biopreserv. Biobank. 17:(4):334–41
     [Crossref] [Google Scholar]
  134. 134.
    Acevedo C, Barfield JP. 2023.. Review: reproductive physiology of bison and application of assisted reproductive technologies to their conservation. . Animal 17:(Suppl. 1):100842
     [Crossref] [Google Scholar]
  135. 135.
    Aune K, Jørgensen D, Gates C. 2016.. Bison bison. . In IUCN Red List of Threatened Species. Gland, Switz:.: Int. Union Conserv. Nat.
     [Google Scholar]
  136. 136.
    Barfield JP. 2019.. In vitro production of bison embryos. . Methods Mol. Biol. 2006.:165–77
     [Google Scholar]
  137. 137.
    Benham HM, McCollum MP, Nol P, Frey RK, Clarke PR, et al. 2021.. Production of embryos and a live offspring using post mortem reproductive material from bison (Bison bison bison) originating in Yellowstone National Park, USA. . Theriogenology 160::33–39
     [Crossref] [Google Scholar]
  138. 138.
    Hussain SA, Lessard C, Anzar M. 2011.. Quantification of damage at different stages of cryopreservation of endangered North American bison (Bison bison) semen and the effects of extender and freeze rate on post-thaw sperm quality. . Anim. Reprod. Sci. 129:(3–4):171–79
     [Crossref] [Google Scholar]
  139. 139.
    Oppenheimer J, Rosen BD, Heaton MP, Vander Ley BL, Shafer WR, et al. 2021.. A reference genome assembly of American bison, Bison bison bison. . J. Hered. 112:(2):174–83
     [Crossref] [Google Scholar]
  140. 140.
    Plumb G, Kowalczyk R, Hernandez-Blanco JA. 2020.. Bison bonasus. . In IUCN Red List of Threatened Species. Gland, Switz.:: Int. Union Conserv. Nat.
     [Google Scholar]
  141. 141.
    Kiewisz J, Melo de Sousa N, Beckers JF, Panasiewicz G, Gizejewski Z, Szafranska B. 2009.. Identification of multiple pregnancy-associated glycoproteins (PAGs) purified from the European bison (Eb; Bison bonasus L.) placentas. . Anim. Reprod. Sci. 112:(3–4):229–50
     [Crossref] [Google Scholar]
  142. 142.
    Duszewska AM, Baraniewicz-Kołek M, Wojdan J, Barłowska K, Bielecki W, et al. 2022.. Establishment of a wisent (Bison bonasus) germplasm bank. . Animals 12:(10):1239
     [Crossref] [Google Scholar]
  143. 143.
    Gardner P, Hedges S, Pudyatmoko S, Gray TNE, Timmins RJ. 2014.. Bos javanicus. . In IUCN Red List of Threatened Species. Gland, Switz:.: Int. Union Conserv. Nat.
     [Google Scholar]
  144. 144.
    Purwantara B, Noor RR, Andersson G, Rodriguez-Martinez H. 2012.. Banteng and Bali cattle in Indonesia: status and forecasts. . Reprod. Domest. Anim. 47:(Suppl. 1):2–6
     [Crossref] [Google Scholar]
  145. 145.
    Sansinena MJ, Hylan D, Hebert K, Denniston RS, Godke RA. 2005.. Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. . Theriogenology 63:(4):1081–91
     [Crossref] [Google Scholar]
  146. 146.
    Steklenev EP, Elistratova TM. 1992.. The characteristics of the reproductive capacity of hybrids of banteng (Bos (Bibos) javanicus d'Alton) with the domestic cow (Bos (Bos) primigenius taurus). . Tsitol. Genet. 26:(6):45–57, 75
     [Google Scholar]
  147. 147.
    Kozlowski CP, Bauman KL, Clawitter HL, Hall R, Poelker C, et al. 2022.. Noninvasive monitoring of steroid hormone production and activity of zoo-housed banteng (Bos javanicus). . Anim. Reprod. Sci. 247::107070
     [Crossref] [Google Scholar]
  148. 148.
    Gillis JD, Holt WV, Yon L, Woad KJ, Love D, et al. 2022.. How can mating systems inform future biobanking strategies? An illustration using two Indonesian bovids, banteng (Bos javanicus) and lowland anoa (Bubalus depressicornis). . Anim. Reprod. Sci. 238::106943
     [Crossref] [Google Scholar]
  149. 149.
    Duckworth JW, Sankar K, Williams AC, Samba Kumar N, Timmins RJ. 2016.. Bos gaurus. . In IUCN Red List of Threatened Species. Gland, Switz:.: Int. Union Conserv. Nat.
     [Google Scholar]
  150. 150.
    Srirattana K, Imsoonthornruksa S, Laowtammathron C, Sangmalee A, Tunwattana W, et al. 2012.. Full-term development of gaur-bovine interspecies somatic cell nuclear transfer embryos: effect of trichostatin A treatment. . Cell. Reprogr. 14:(3):248–57
     [Crossref] [Google Scholar]
  151. 151.
    Imsoonthornruksa S, Srirattana K, Phewsoi W, Tunwattana W, Parnpai R, Ketudat-Cairns M. 2012.. Segregation of donor cell mitochondrial DNA in gaur-bovine interspecies somatic cell nuclear transfer embryos, fetuses and an offspring. . Mitochondrion 12:(5):506–13
     [Crossref] [Google Scholar]
  152. 152.
    Mastromonaco GF, Favetta LA, Smith LC, Filion F, King WA. 2007.. The influence of nuclear content on developmental competence of gaur × cattle hybrid in vitro fertilized and somatic cell nuclear transfer embryos. . Biol. Reprod. 76:(3):514–23
     [Crossref] [Google Scholar]
  153. 153.
    Humble E, Stoffel MA, Dicks K, Ball AD, Gooley RM, et al. 2023.. Conservation management strategy impacts inbreeding and mutation load in scimitar-horned oryx. . PNAS 120:(18):e2210756120
     [Crossref] [Google Scholar]
  154. 154.
    Woodfine T, Gilbert T. 2016.. The fall and rise of the scimitar-horned oryx. . In Antelope Conservation, ed. J Bro-Jørgensen, DP Mallon , pp. 280–96. Hoboken, NJ:: John Wiley & Sons
     [Google Scholar]
  155. 155.
    Fitzgerald HC, Schust DJ, Spencer TE. 2021.. In vitro models of the human endometrium: evolution and application for women's health. . Biol. Reprod. 104:(2):282–93
     [Crossref] [Google Scholar]
  156. 156.
    Pinzón-Arteaga CA, Wang Y, Wei Y, Ribeiro Orsi AE, Li L, et al. 2023.. Bovine blastocyst-like structures derived from stem cell cultures. . Cell Stem Cell 30:(5):611–16.e7
     [Crossref] [Google Scholar]
  157. 157.
    Rivron NC, Frias-Aldeguer J, Vrij EJ, Boisset J-C, Korving J, et al. 2018.. Blastocyst-like structures generated solely from stem cells. . Nature 557:(7703):106–11
     [Crossref] [Google Scholar]
  158. 158.
    Yu L, Wei Y, Duan J, Schmitz DA, Sakurai M, et al. 2021.. Blastocyst-like structures generated from human pluripotent stem cells. . Nature 591:(7851):620–26
     [Crossref] [Google Scholar]
  159. 159.
    Brandão DO, Maddox-Hyttel P, Løvendahl P, Rumpf R, Stringfellow D, Callesen H. 2004.. Post hatching development: a novel system for extended in vitro culture of bovine embryos. . Biol. Reprod. 71:(6):2048–55
     [Crossref] [Google Scholar]
  160. 160.
    Vajta G, Alexopoulos NI, Callesen H. 2004.. Rapid growth and elongation of bovine blastocysts in vitro in a three-dimensional gel system. . Theriogenology 62:(7):1253–63
     [Crossref] [Google Scholar]
  161. 161.
    Ramos-Ibeas P, Lamas-Toranzo I, Martínez-Moro Á, de Frutos C, Quiroga AC, et al. 2020.. Embryonic disc formation following post-hatching bovine embryo development in vitro. . Reproduction 160:(4):579–89
     [Crossref] [Google Scholar]
  162. 162.
    Sugino Y, Sato T, Yamamoto Y, Kimura K. 2022.. Evaluation of bovine uterine gland functions in 2D and 3D culture system. . J. Reprod. Dev. 68:(4):254–61
     [Crossref] [Google Scholar]
  163. 163.
    Díez MC, Przyborski S, del Cerro A, Alonso-Guervós M, Iglesias-Cabo T, et al. 2023.. Generation of a novel three-dimensional scaffold-based model of the bovine endometrium. . Vet. Res. Commun. 47:(3):1721–33
     [Crossref] [Google Scholar]
  164. 164.
    Hill DS, Robinson NDP, Caley MP, Chen M, O'Toole EA, et al. 2015.. A novel fully humanized 3D skin equivalent to model early melanoma invasion. . Mol. Cancer Ther. 14:(11):2665–73
     [Crossref] [Google Scholar]
  165. 165.
    Costello L, Fullard N, Roger M, Bradbury S, Dicolandrea T, et al. 2019.. Engineering a multilayered skin equivalent: the importance of endogenous extracellular matrix maturation to provide robustness and reproducibility. . In Skin Tissue Engineering: Methods and Protocols, ed. S Böttcher-Haberzeth, T Biedermann , pp. 107–22. New York:: Springer
     [Google Scholar]
  166. 166.
    Totti S, Ng KW, Dale L, Lian G, Chen T, Velliou EG. 2019.. A novel versatile animal-free 3D tool for rapid low-cost assessment of immunodiagnostic microneedles. . Sens. Actuators B 296::126652
     [Crossref] [Google Scholar]
  167. 167.
    Arslan SY, Yu Y, Burdette JE, Pavone ME, Hope TJ, et al. 2015.. Novel three dimensional human endocervix cultures respond to 28-day hormone treatment. . Endocrinology 156:(4):1602–9
     [Crossref] [Google Scholar]
  168. 168.
    De Bem THC, Tinning H, Vasconcelos EJR, Wang D, Forde N. 2021.. Endometrium-on-a-chip reveals insulin- and glucose-induced alterations in the transcriptome and proteomic secretome. . Endocrinology 162:(6):bqab054
     [Crossref] [Google Scholar]
  169. 169.
    Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, et al. 2017.. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. . Nat. Commun. 8::14584
     [Crossref] [Google Scholar]
  170. 170.
    Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, et al. 2017.. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. . Nat. Cell Biol. 19:(5):568–77
     [Crossref] [Google Scholar]
  171. 171.
    Cindrova-Davies T, Zhao X, Elder K, Jones CJP, Moffett A, et al. 2021.. Menstrual flow as a non-invasive source of endometrial organoids. . Commun. Biol. 4::651
     [Crossref] [Google Scholar]
  172. 172.
    Kawasaki M, Dykstra GD, McConnel CS, Burbick CR, Ambrosini YM. 2023.. Adult bovine-derived small and large intestinal organoids: in vitro development and maintenance. . J. Tissue Eng. Regen. Med. 2023::e3095002
     [Crossref] [Google Scholar]
  173. 173.
    Yamauchi N, Yamada O, Takahashi T, Imai K, Sato T, et al. 2003.. A three-dimensional cell culture model for bovine endometrium: regeneration of a multicellular spheroid using ascorbate. . Placenta 24:(2–3):258–69
     [Crossref] [Google Scholar]
  174. 174.
    Lawson EF, Ghosh A, Blanch V, Grupen CG, Aitken RJ, et al. 2023.. Establishment and characterization of oviductal organoids from farm and companion animals. . Biol. Reprod. 108:(6):854–65
     [Crossref] [Google Scholar]
  175. 175.
    Turco MY, Gardner L, Kay RG, Hamilton RS, Prater M, et al. 2018.. Trophoblast organoids as a model for maternal-fetal interactions during human placentation. . Nature 564:(7735):263–67
     [Crossref] [Google Scholar]
  176. 176.
    Davenport KM, O'Neil EV, Ortega MS, Patterson A, Kelleher AM, et al. 2024.. Single-cell insights into development of the bovine placenta. . Biol. Reprod. 110:(1):169–84
     [Crossref] [Google Scholar]
  177. 177.
    Garcia-Flores V, Romero R, Tarca AL, Peyvandipour A, Xu Y, et al. 2024.. Deciphering maternal-fetal cross-talk in the human placenta during parturition using single-cell RNA sequencing. . Sci. Transl. Med. 16:(729):eadh8335
     [Crossref] [Google Scholar]
  178. 178.
    Ming H, Zhang M, Rajput S, Logsdon D, Zhu L, et al. 2024.. In vitro culture alters cell lineage composition and cellular metabolism of bovine blastocyst. . Biol. Reprod. 111::11–27
     [Crossref] [Google Scholar]
  179. 179.
    Butt Z, Tinning H, O'Connell MJ, Fenn J, Alberio R, Forde N. 2023.. Understanding conceptus-maternal interactions: What tools do we need to develop?. Reprod. Fertil. Dev. 36:(2):81–92
     [Crossref] [Google Scholar]
  180. 180.
    Adhikari B, Lee CN, Khadka VS, Deng Y, Fukumoto G, et al. 2022.. RNA-sequencing based analysis of bovine endometrium during the maternal recognition of pregnancy. . BMC Genom. 23::494
     [Crossref] [Google Scholar]
  181. 181.
    Kues WA, Sudheer S, Herrmann D, Carnwath JW, Havlicek V, et al. 2008.. Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. . PNAS 105:(50):19768–73
     [Crossref] [Google Scholar]
  182. 182.
    Mamo S, Mehta JP, McGettigan P, Fair T, Spencer TE, et al. 2011.. RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. . Biol. Reprod. 85:(6):1143–51
     [Crossref] [Google Scholar]
  183. 183.
    Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. 2014.. Fine mapping of genome activation in bovine embryos by RNA sequencing. . PNAS 111:(11):4139–44
     [Crossref] [Google Scholar]
  184. 184.
    Schalich KM, Koganti PP, Castillo JM, Reiff OM, Cheong SH, Selvaraj V. 2024.. The uterine secretory cycle: recurring physiology of endometrial outputs that setup the uterine luminal microenvironment. . Physiol. Genom. 56:(1):74–97
     [Crossref] [Google Scholar]
  185. 185.
    Palma-Vera SE, Sharbati S, Einspanier R. 2015.. Identification of miRNAs in bovine endometrium through RNAseq and prediction of regulated pathways. . Reprod. Domest. Anim. 50:(5):800–6
     [Crossref] [Google Scholar]
  186. 186.
    Yan C, Lv H, Peng Z, Yang D, Shen P, et al. 2021.. Analysis of miRNA expression changes in bovine endometrial stromal cells treated with lipopolysaccharide. . Theriogenology 167::85–93
     [Crossref] [Google Scholar]
  187. 187.
    Cuthbert JM, Russell SJ, Polejaeva IA, Meng Q, White KL, Benninghoff AD. 2021.. Dynamics of small non-coding RNAs in bovine scNT embryos through the maternal-to-embryonic transition. . Biol. Reprod. 105:(4):918–33
     [Crossref] [Google Scholar]
  188. 188.
    Salilew-Wondim D, Tholen E, Held-Hoelker E, Shellander K, Blaschka C, et al. 2024.. Endometrial DNA methylation signatures during the time of breeding in relation to the pregnancy outcome in postpartum dairy cows fed a control diet or supplemented with rumen-protected methionine. . Front. Genet. 14::1267053
     [Crossref] [Google Scholar]
  189. 189.
    Chen Z, Hagen DE, Wang J, Elsik CG, Ji T, et al. 2016.. Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing. . Epigenetics 11:(7):501–16
     [Crossref] [Google Scholar]
  190. 190.
    Rabaglino MB, O'Doherty A, Bojsen-Møller Secher J, Lonergan P, Hyttel P, et al. 2021.. Application of multi-omics data integration and machine learning approaches to identify epigenetic and transcriptomic differences between in vitro and in vivo produced bovine embryos. . PLOS ONE 16:(5):e0252096
     [Crossref] [Google Scholar]
  191. 191.
    Choe C, Park J-W, Kim E-S, Lee S-G, Park S-Y, et al. 2010.. Proteomic analysis of differentially expressed proteins in bovine endometrium with endometritis. . Korean J. Physiol. Pharmacol. 14:(4):205–12
     [Crossref] [Google Scholar]
  192. 192.
    Piras C, Guo Y, Soggiu A, Chanrot M, Greco V, et al. 2017.. Changes in protein expression profiles in bovine endometrial epithelial cells exposed to E. coli LPS challenge. . Mol. BioSyst. 13:(2):392–405
     [Crossref] [Google Scholar]
  193. 193.
    Banliat C, Mahé C, Lavigne R, Com E, Pineau C, et al. 2022.. The proteomic analysis of bovine embryos developed in vivo or in vitro reveals the contribution of the maternal environment to early embryo. . BMC Genom. 23::839
     [Crossref] [Google Scholar]
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Ruminating on Bovine Implantation: Its Importance in Fertility, Food Production, Conservation, and Health
Annual Review of Animal Biosciences 13, 143 (2025); https://doi.org/10.1146/annurev-animal-111523-102403
/content/journals/10.1146/annurev-animal-111523-102403
/content/journals/10.1146/annurev-animal-111523-102403
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