Animal Reproduction (AR)
Animal Reproduction (AR)

Endometrial receptivity in cattle: the mutual reprogramming paradigm

Mario Binelli; Felipe Alves Correa Carvalho Silva; Cecilia Constantino Rocha; Thiago Martins; Mariana Sponchiado; Veerle Van Hoeck; Andrey Cordeiro; Meghan Campbell; Jo L. M. R. Leroy; Francisco Peñagaricano; Guilherme Pugliesi

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Prior to implantation in cattle, the mucous medium contained in the uterine lumen serves as a working interface for molecular exchange and signaling between the lining endometrium and the embryo. The composition of this luminal fluid changes temporally according to the secretory and reabsorptive activities of the uterus and the embryo, which are under complex regulation. Via this interface, both the embryo and the endometrium reprogram each other’s functions to support pregnancy continuation beyond the pre-implantation period. More specifically, the embryo receives elongation signals and the uterus receives anti-luteolytic stimuli. Here, characteristics of the luminal compartment as well as the regulation of its composition to determine the pregnancy outcome will be discussed.


cattle, endometrium, sex-steroids, embryo


Belaz KRA, Tata A, França MR, Silva MIS, Vendramini PH, Fernandes AMAP, D’Alexandri FL, Eberlin MN, Binelli M. Phospholipid profile and distribution in the receptive oviduct and uterus during early diestrus in cattle1. Biol Reprod. 2016;95(6):127. PMid:27760751.

Cardoso B, Oliveira ML, Pugliesi G, Batista EOS, Binelli M. Cytobrush: a tool for sequential evaluation of gene expression in bovine endometrium. Reprod Domest Anim. 2017;52(6):1153-7. PMid:28755420.

França MR, Mesquita FS, Lopes E, Pugliesi G, Van Hoeck V, Chiaratti MR, Membrive CB, Papa PC, Binelli M. Modulation of periovulatory endocrine profiles in beef cows: consequences for endometrial glucose transporters and uterine fluid glucose levels. Domest Anim Endocrinol. 2015;50:83-90. PMid:25447883.

França MR, Silva MIS, Pugliesi G, Van Hoeck V, Binelli M. Evidence of endometrial amino acid metabolism and transport modulation by peri-ovulatory endocrine profiles driving uterine receptivity. J Anim Sci Biotechnol. 2017;8(1):54. PMid:28630707.

Gao H, Wu G, Spencer TE, Johnson GA, Bazer FW. Select nutrients in the ovine uterine lumen. II. Glucose transporters in the uterus and peri-implantation Conceptuses1. Biol Reprod. 2009;80(1):94-104. PMid:18753604.

Hansen PJ. The incompletely fulfilled promise of embryo transfer in cattle-why aren’t pregnancy rates greater and what can we do about it? J Anim Sci. 2020;98(11):skaa288. PMid:33141879.

Jinks EM, Smith MF, Atkins JA, Pohler KG, Perry GA, Macneil MD, Roberts AJ, Waterman RC, Alexander LJ, Geary TW. Preovulatory estradiol and the establishment and maintenance of pregnancy in suckled beef cows. J Anim Sci. 2013;91(3):1176-85. PMid:23296810.

Martins T, Pugliesi G, Sponchiado M, Gonella-Diaza AM, Ojeda-Rojas OA, Rodriguez FD, Ramos RS, Basso AC, Binelli M. Perturbations in the uterine luminal fluid composition are detrimental to pregnancy establishment in cattle. J Anim Sci Biotechnol. 2018;9(1):70. PMid:30356865.

Martins T, Sponchiado M, Silva FACC, Estrada-Cortés E, Hansen PJ, Peñagaricano F, Binelli M. Progesterone-dependent and progesterone-independent modulation of luminal epithelial transcription to support pregnancy in cattle. Physiol Genomics. 2022;54(2):71-85. PMid:34890509.

Mesquita FS, Pugliesi G, Scolari SC, Franca MR, Ramos RS, Oliveira M, Papa PC, Bressan FF, Meirelles FV, Silva LA, Nogueira GP, Membrive CM, Binelli M. Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows. Theriogenology. 2014;81(6):861-9. PMid:24507960.

Mesquita FS, Ramos RS, Pugliesi G, Andrade SCS, Van Hoeck V, Langbeen A, Oliveira ML, Gonella-Diaza AM, Gasparin G, Fukumasu H, Pulz LH, Membrive CM, Coutinho LL, Binelli M. The receptive endometrial transcriptomic signature indicates an earlier shift from proliferation to metabolism at early diestrus in the cow. Biol Reprod. 2015;93(2):52. PMid:26178716.

Pierson RA, Ginther OJ. Ultrasonographic appearance of the bovine uterus during the estrous cycle. J Am Vet Med Assoc. 1987;190(8):995-1001. PMid:3570959.

Pugliesi G, Santos FB, Lopes E, Nogueira E, Maio JRG, Binelli M. Improved fertility in suckled beef cows ovulating large follicles or supplemented with long-acting progesterone after timed-AI. Theriogenology. 2016;85(7):1239-48. PMid:26764150.

Ramos RS, Oliveira ML, Izaguirry AP, Vargas LM, Soares MB, Mesquita FS, Santos FW, Binelli M. The periovulatory endocrine milieu affects the uterine redox environment in beef cows. Reprod Biol Endocrinol. 2015;13(1):39. PMid:25957795.

Reese ST, Franco GA, Poole RK, Hood R, Montero LF, Oliveira RV Fo, Cooke RF, Pohler KG. Pregnancy loss in beef cattle: a meta-analysis. Anim Reprod Sci. 2020;212:106251. PMid:31864492.

Rocha CC, Silva FAC, Martins T, Marrero MG, Bromfield JJ, Driver J, Hansen T, Oliveira L, Binelli M. Culture of endometrial epithelial cells collected by a cytological brush in vivo. JDS Commun. 2022;3(3):217-21. PMid:36338819.

Sá MF Fo, Gonella-Diaza AM, Sponchiado M, Mendanha MF, Pugliesi G, Ramos RDS, Andrade SCDS, Gasparin G, Coutinho LL, Goissis MD, Mesquita FS, Baruselli PS, Binelli M. Impact of hormonal modulation at proestrus on ovarian responses and uterine gene expression of suckled anestrous beef cows. J Anim Sci Biotechnol. 2017;8(1):79. PMid:29118976.

Santos ÉC, Fonseca AM Jr, Lima CB, Ispada J, Silva JVA, Milazzotto MP. Less is more: reduced nutrient concentration during in vitro culture improves embryo production rates and morphophysiology of bovine embryos. Theriogenology. 2021;173:37-47. PMid:34329894.

Scolari SC, Pugliesi G, Strefezzi RF, Andrade SC, Coutinho LL, Binelli M. Dynamic remodeling of endometrial extracellular matrix regulates embryo receptivity in cattle. Reproduction. 2017;153(1):49-61. PMid:27754873.

Shirasuna K, Asaoka H, Acosta TJ, Wijayagunawardane MPB, Ohtani M, Hayashi K-G, Matsui M, Miyamoto A. Real-time dynamics of prostaglandin F2alpha release from uterus and corpus luteum during spontaneous luteolysis in the cow. Reproduction. 2004;128(2):189-95. PMid:15280558.

Silva FACC, Silva GF, Vieira BS, Laurindo A No, Rocha CC, Turco EG, Nogueira GP, Pugliesi G, Binelli M. Peri-estrus ovarian, uterine, and hormonal variables determine the uterine luminal fluid metabolome in beef heifers. Biol Reprod. 2021;105(5):1140-53. PMid:34350935.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. The influence of progesterone on bovine uterine fluid energy, nucleotide, vitamin, cofactor, peptide, and xenobiotic composition during the conceptus elongation-initiation window. Sci Rep. 2019a;9(1):7716. PMid:31118434.

Simintiras CA, Sánchez JM, McDonald M, Martins T, Binelli M, Lonergan P. Biochemical characterization of progesterone-induced alterations in bovine uterine fluid amino acid and carbohydrate composition during the conceptus elongation window†. Biol Reprod. 2019b;100(3):672-85. PMid:30388203.

Thatcher WW, Guzeloglu A, Mattos R, Binelli M, Hansen TR, Pru JK. Uterine-conceptus interactions and reproductive failure in cattle. Theriogenology. 2001;56(9):1435-50. PMid:11768809.

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