Analyze Diet
International journal of molecular sciences2020; 21(7); 2562; doi: 10.3390/ijms21072562

Asynchronous Embryo Transfer Followed by Comparative Transcriptomic Analysis of Conceptus Membranes and Endometrium Identifies Processes Important to the Establishment of Equine Pregnancy.

Abstract: Preimplantation horse conceptuses require nutrients and signals from histotroph, the composition of which is regulated by luteal progesterone and conceptus-secreted factors. To distinguish progesterone and conceptus effects we shortened the period of endometrial progesterone-priming by asynchronous embryo transfer. Day 8 embryos were transferred to synchronous (day 8) or asynchronous (day 3) recipients, and RNA sequencing was performed on endometrium and conceptuses recovered 6 and 11 days later (embryo days 14 and 19). Asynchrony resulted in many more differentially expressed genes (DEGs) in conceptus membranes (3473) than endometrium (715). Gene ontology analysis identified upregulation in biological processes related to organogenesis and preventing apoptosis in synchronous conceptuses on day 14, and in cell adhesion and migration on day 19. Asynchrony also resulted in large numbers of DEGs related to 'extracellular exosome'. In endometrium, genes involved in immunity, the inflammatory response, and apoptosis regulation were upregulated during synchronous pregnancy and, again, many genes related to extracellular exosome were differentially expressed. Interestingly, only 14 genes were differentially expressed in endometrium recovered 6 days after synchronous versus 11 days after asynchronous transfer (day 14 recipient in both). Among these, and were consistently upregulated in synchronous endometrium. Furthermore bradykinin, an active peptide cleaved from KNG1, stimulated prostaglandin release by cultured trophectoderm cells. The horse conceptus thus responds to a negatively asynchronous uterus by extensively adjusting its transcriptome, whereas the endometrial transcriptome is modified only subtly by a more advanced conceptus.
Publication Date: 2020-04-07 PubMed ID: 32272720PubMed Central: PMC7177982DOI: 10.3390/ijms21072562Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research explores how preimplantation horse embryos adjust their gene expression in response to changes in the maturational status of the uterus. By transferring a Day 8 embryo into a Day 3 uterus (asynchronous) versus a Day 8 uterus (synchronous), the researchers found significant differences in gene expression between the two scenarios, providing insights into the processes important for the establishment of equine pregnancy.

Research Methodology

  • The research was undertaken by extrapolating Day 8 horse embryos and implanting them into synchronous (Day 8) uterine environment or into asynchronous (Day 3) uterine environment.
  • RNA sequencing was then conducted on both the endometrium (uterine lining) and the embryos themselves (conceptuses), 6 and 11 days post-implantation, corresponding to Days 14 and 19 of the embryo’s development.

Findings and Interpretations

  • The results showed that the state of asynchrony led to more differentially expressed genes (DEGs) in the conceptus membranes (3,473 genes) than in the endometrium (715 genes).
  • Gene ontology analysis was also performed to understand the biological functions of these DEGs. Findings showed upregulation of processes related to organ development and apoptosis prevention in conceptuses in a synchronous environment on Day 14. By Day 19, cell adhesion and migration processes were prominent.
  • The asynchronous environment led to significant changes in gene expression related to ‘extracellular exosome’, a type of cell communication.
  • The endometrium also showed altered gene expression during synchronous pregnancy, including upregulation of genes involved in immune response, inflammation, and apoptosis regulation. The changes in the endometrium were more subtle than in the conceptus.
  • Only 14 genes were differentially expressed in the endometrium when comparing Day 6 synchronously transferred embryos to Day 11 asynchronously transferred embryos. Two genes, KNG1 and CYP19A1, were consistently upregulated in the synchronous environment.

Implications and Conclusions

  • The research thus concludes that the horse conceptus adapts to an environmentally mismatched uterus by extensively modifying its gene expression. The uterus, in contrast, adjusts its gene expression minimally in response to a more advanced conceptus.
  • The upregulation of specific genes like KNG1 (which encodes bradykinin) also highlight potential communication pathways between the endometrium and conceptus. This could help in understanding and improving equine pregnancy outcomes.

Cite This Article

APA
Gibson C, de Ruijter-Villani M, Bauersachs S, Stout TAE. (2020). Asynchronous Embryo Transfer Followed by Comparative Transcriptomic Analysis of Conceptus Membranes and Endometrium Identifies Processes Important to the Establishment of Equine Pregnancy. Int J Mol Sci, 21(7), 2562. https://doi.org/10.3390/ijms21072562

Publication

ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 21
Issue: 7
PII: 2562

Researcher Affiliations

Gibson, Charlotte
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The Netherlands.
de Ruijter-Villani, Marta
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The Netherlands.
Bauersachs, Stefan
  • Institute of Veterinary Anatomy, Vetsuisse Faculty Zurich, University of Zurich, 8315 Lindau (ZH), Switzerland.
Stout, Tom A E
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The Netherlands.

MeSH Terms

  • Animals
  • Apoptosis / physiology
  • Embryo Transfer / methods
  • Embryo, Mammalian / metabolism
  • Embryo, Mammalian / physiology
  • Embryonic Development / physiology
  • Endometrium / metabolism
  • Endometrium / physiology
  • Female
  • Horses
  • Membranes / metabolism
  • Membranes / physiology
  • Pregnancy
  • Transcriptome / physiology
  • Up-Regulation / physiology
  • Uterus / metabolism
  • Uterus / physiology

Grant Funding

  • PITN-GA-2012-317146-EpiHealthNet / FP7 People: Marie-Curie Actions

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 80 references
  1. Stout TA. Embryo-maternal communication during the first 4 weeks of equine pregnancy.. Theriogenology 2016 Jul 1;86(1):349-54.
  2. Freeman DA, Weber JA, Geary RT, Woods GL. Time of embryo transport through the mare oviduct.. Theriogenology 1991 Nov;36(5):823-30.
    doi: 10.1016/0093-691X(91)90348-Hpubmed: 16727051google scholar: lookup
  3. Allen WR, Stewart F. Equine placentation.. Reprod Fertil Dev 2001;13(7-8):623-34.
    doi: 10.1071/RD01063pubmed: 11999314google scholar: lookup
  4. Oriol JG, Sharom FJ, Betteridge KJ. Developmentally regulated changes in the glycoproteins of the equine embryonic capsule.. J Reprod Fertil 1993 Nov;99(2):653-64.
    doi: 10.1530/jrf.0.0990653pubmed: 8107051google scholar: lookup
  5. Herrler A, Stewart F, Crossett B, Pell JM, Ellis PD, Beier HM, Allen WR. Identification of proteins in the equine embryonic capsule.. J Reprod Fertil Suppl 2000;(56):601-6.
    pubmed: 20681175
  6. Ginther OJ. Intrauterine movement of the early conceptus in barren and postpartum mares.. Theriogenology 1984 Apr;21(4):633-44.
    doi: 10.1016/0093-691X(84)90460-6pubmed: 16725913google scholar: lookup
  7. McDowell KJ, Sharp DC, Grubaugh W, Thatcher WW, Wilcox CJ. Restricted conceptus mobility results in failure of pregnancy maintenance in mares.. Biol Reprod 1988 Sep;39(2):340-8.
    doi: 10.1095/biolreprod39.2.340pubmed: 3179385google scholar: lookup
  8. Starbuck GR, Stout TA, Lamming GE, Allen WR, Flint AP. Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy.. J Reprod Fertil 1998 Jul;113(2):173-9.
    doi: 10.1530/jrf.0.1130173pubmed: 9861156google scholar: lookup
  9. Stout TA, Allen WR. Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares.. Reproduction 2002 Feb;123(2):261-8.
    doi: 10.1530/rep.0.1230261pubmed: 11866693google scholar: lookup
  10. Goff AK, Pontbriand D, Sirois J. Oxytocin stimulation of plasma 15-keto-13,14-dihydro prostaglandin F-2 alpha during the oestrous cycle and early pregnancy in the mare.. J Reprod Fertil Suppl 1987;35:253-60.
    pubmed: 3479581
  11. Stout TA, Lamming GE, Allen WR. Oxytocin administration prolongs luteal function in cyclic mares.. J Reprod Fertil 1999 Jul;116(2):315-20.
    doi: 10.1530/jrf.0.1160315pubmed: 10615256google scholar: lookup
  12. Klein C, Troedsson MH. Maternal recognition of pregnancy in the horse: a mystery still to be solved.. Reprod Fertil Dev 2011;23(8):952-63.
    doi: 10.1071/RD10294pubmed: 22127001google scholar: lookup
  13. de Ruijter-Villani M, van Tol HT, Stout TA. Effect of pregnancy on endometrial expression of luteolytic pathway components in the mare.. Reprod Fertil Dev 2015 Jun;27(5):834-45.
    doi: 10.1071/RD13381pubmed: 24679480google scholar: lookup
  14. Merkl M, Ulbrich SE, Otzdorff C, Herbach N, Wanke R, Wolf E, Handler J, Bauersachs S. Microarray analysis of equine endometrium at days 8 and 12 of pregnancy.. Biol Reprod 2010 Nov;83(5):874-86.
    doi: 10.1095/biolreprod.110.085233pubmed: 20631402google scholar: lookup
  15. Bauersachs S, Wolf E. Transcriptome analyses of bovine, porcine and equine endometrium during the pre-implantation phase.. Anim Reprod Sci 2012 Sep;134(1-2):84-94.
  16. Klohonatz KM, Coleman SJ, Islas-Trejo AD, Medrano JF, Hess AM, Kalbfleisch T, Thomas MG, Bouma GJ, Bruemmer JE. Coding RNA Sequencing of Equine Endometrium during Maternal Recognition of Pregnancy.. Genes (Basel) 2019 Sep 25;10(10).
    doi: 10.3390/genes10100749pmc: PMC6826732pubmed: 31557877google scholar: lookup
  17. Klohonatz KM, Hess AM, Hansen TR, Squires EL, Bouma GJ, Bruemmer JE. Equine endometrial gene expression changes during and after maternal recognition of pregnancy.. J Anim Sci 2015 Jul;93(7):3364-76.
    doi: 10.2527/jas.2014-8826pubmed: 26440005google scholar: lookup
  18. Klein C, Scoggin KE, Ealy AD, Troedsson MH. Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.. Biol Reprod 2010 Jul;83(1):102-13.
    doi: 10.1095/biolreprod.109.081612pubmed: 20335638google scholar: lookup
  19. Klein C, Troedsson MH. Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse.. Biol Reprod 2011 May;84(5):872-85.
    doi: 10.1095/biolreprod.110.088732pubmed: 21209420google scholar: lookup
  20. Klein C. Novel equine conceptus?endometrial interactions on Day 16 of pregnancy based on RNA sequencing.. Reprod Fertil Dev 2015 May 5;.
    doi: 10.1071/RD14489pubmed: 25940503google scholar: lookup
  21. Swegen A, Grupen CG, Gibb Z, Baker MA, de Ruijter-Villani M, Smith ND, Stout TAE, Aitken RJ. From Peptide Masses to Pregnancy Maintenance: A Comprehensive Proteomic Analysis of The Early Equine Embryo Secretome, Blastocoel Fluid, and Capsule.. Proteomics 2017 Sep;17(17-18).
    doi: 10.1002/pmic.201600433pubmed: 28782881google scholar: lookup
  22. Smits K, Willems S, Van Steendam K, Van De Velde M, De Lange V, Ververs C, Roels K, Govaere J, Van Nieuwerburgh F, Peelman L, Deforce D, Van Soom A. Proteins involved in embryo-maternal interaction around the signalling of maternal recognition of pregnancy in the horse.. Sci Rep 2018 Mar 27;8(1):5249.
    doi: 10.1038/s41598-018-23537-6pmc: PMC5869742pubmed: 29588480google scholar: lookup
  23. Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation.. Reproduction 2009 Aug;138(2):195-209.
    doi: 10.1530/REP-09-0158pubmed: 19502456google scholar: lookup
  24. Filant J, Spencer TE. Uterine glands: biological roles in conceptus implantation, uterine receptivity and decidualization.. Int J Dev Biol 2014;58(2-4):107-16.
    doi: 10.1387/ijdb.130344tspmc: PMC4199233pubmed: 25023676google scholar: lookup
  25. Lonergan P, Forde N. The role of pogesterone in maternal recognition of pregnancy in domestic ruminants. Regulation of Implantation and Establishment of Pregnancy in Mammals 2015;pp. 87–104.
  26. Satterfield MC, Hayashi K, Song G, Black SG, Bazer FW, Spencer TE. Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus.. Biol Reprod 2008 Dec;79(6):1226-36.
    doi: 10.1095/biolreprod.108.071787pubmed: 18753603google scholar: lookup
  27. Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O'Gaora P, Lonergan P, Roche JF. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle.. Biol Reprod 2009 Oct;81(4):784-94.
    doi: 10.1095/biolreprod.108.074336pubmed: 19553605google scholar: lookup
  28. Spencer TE, Forde N, Lonergan P. The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants.. J Dairy Sci 2016 Jul;99(7):5941-5950.
    doi: 10.3168/jds.2015-10070pubmed: 26387021google scholar: lookup
  29. Allen WR, Mathias S, Lennard SN, Greenwood RE. Serial measurement of peripheral oestrogen and progesterone concentrations in oestrous mares to determine optimum mating time and diagnose ovulation.. Equine Vet J 1995 Nov;27(6):460-4.
  30. Mann GE, Lamming GE. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows.. Reproduction 2001 Jan;121(1):175-80.
    doi: 10.1530/rep.0.1210175pubmed: 11226041google scholar: lookup
  31. Willmann C, Budik S, Walter I, Aurich C. Influences of treatment of early pregnant mares with the progestin altrenogest on embryonic development and gene expression in the endometrium and conceptus.. Theriogenology 2011 Jul 1;76(1):61-73.
  32. Beyer T, Rink BE, Scarlet D, Walter I, Kunert S, Aurich C. Early luteal phase progestin concentration influences endometrial function in pregnant mares.. Theriogenology 2019 Feb;125:236-241.
  33. Randi F, Fernandez-Fuertes B, McDonald M, Forde N, Kelly AK, Bastos Amorin H, Muniz de Lima E, Morotti F, Marcondes Seneda M, Lonergan P. Asynchronous embryo transfer as a tool to understand embryo-uterine interaction in cattle: is a large conceptus a good thing?. Reprod Fertil Dev 2016 Oct;28(12):1999-2006.
    doi: 10.1071/RD15195pubmed: 26220578google scholar: lookup
  34. Geisert RD, Fox TC, Morgan GL, Wells ME, Wettemann RP, Zavy MT. Survival of bovine embryos transferred to progesterone-treated asynchronous recipients.. J Reprod Fertil 1991 Jul;92(2):475-82.
    doi: 10.1530/jrf.0.0920475pubmed: 1886103google scholar: lookup
  35. Ledgard AM, Berg MC, McMillan WH, Smolenski G, Peterson AJ. Effect of asynchronous transfer on bovine embryonic development and relationship with early cycle uterine proteome profiles.. Reprod Fertil Dev 2012;24(7):962-72.
    doi: 10.1071/RD11225pubmed: 22935157google scholar: lookup
  36. Wilsher S, Clutton-Brock A, Allen WR. Successful transfer of day 10 horse embryos: influence of donor-recipient asynchrony on embryo development.. Reproduction 2010 Mar;139(3):575-85.
    doi: 10.1530/REP-09-0306pubmed: 19948839google scholar: lookup
  37. Jacob JC, Haag KT, Santos GO, Oliveira JP, Gastal MO, Gastal EL. Effect of embryo age and recipient asynchrony on pregnancy rates in a commercial equine embryo transfer program.. Theriogenology 2012 Apr 1;77(6):1159-66.
  38. Cuervo-Arango J, Claes AN, Stout TAE. In vitro-produced horse embryos exhibit a very narrow window of acceptable recipient mare uterine synchrony compared with in vivo-derived embryos.. Reprod Fertil Dev 2019 Jan;31(12):1904-1911.
    doi: 10.1071/RD19294pubmed: 31587698google scholar: lookup
  39. Wilsher S, Allen WR. Uterine influences on embryogenesis and early placentation in the horse revealed by transfer of day 10 embryos to day 3 recipient mares.. Reproduction 2009 Mar;137(3):583-93.
    doi: 10.1530/REP-08-0328pubmed: 19074502google scholar: lookup
  40. Gibson C, de Ruijter-Villani M, Stout TAE. Negative uterine asynchrony retards early equine conceptus development and upregulation of placental imprinted genes.. Placenta 2017 Sep;57:175-182.
  41. Gibson C, de Ruijter-Villani M, Rietveld J, Stout TAE. Amino acid transporter expression in the endometrium and conceptus membranes during early equine pregnancy.. Reprod Fertil Dev 2018 Nov;30(12):1675-1688.
    doi: 10.1071/RD17352pubmed: 29903343google scholar: lookup
  42. Gibson C, de Ruijter-Villani M, Rietveld J, Stout TAE. Expression of glucose transporters in the endometrium and early conceptus membranes of the horse.. Placenta 2018 Aug;68:23-32.
  43. Burns GW, Brooks KE, Spencer TE. Extracellular Vesicles Originate from the Conceptus and Uterus During Early Pregnancy in Sheep.. Biol Reprod 2016 Mar;94(3):56.
    doi: 10.1095/biolreprod.115.134973pubmed: 26819476google scholar: lookup
  44. Burns GW, Brooks KE, O'Neil EV, Hagen DE, Behura SK, Spencer TE. Progesterone effects on extracellular vesicles in the sheep uterus.. Biol Reprod 2018 May 1;98(5):612-622.
    doi: 10.1093/biolre/ioy011pubmed: 29346527google scholar: lookup
  45. Quinn BA, Hayes MA, Waelchli RO, Kennedy MW, Betteridge KJ. Changes in major proteins in the embryonic capsule during immobilization (fixation) of the conceptus in the third week of pregnancy in the mare.. Reproduction 2007 Jul;134(1):161-70.
    doi: 10.1530/REP-06-0241pubmed: 17641098google scholar: lookup
  46. Crossett B, Allen WR, Stewart F. A 19 kDa protein secreted by the endometrium of the mare is a novel member of the lipocalin family.. Biochem J 1996 Nov 15;320 ( Pt 1)(Pt 1):137-43.
    doi: 10.1042/bj3200137pmc: PMC1217908pubmed: 8947478google scholar: lookup
  47. Allen WR, Gower S, Wilsher S. Immunohistochemical localization of vascular endothelial growth factor (VEGF) and its two receptors (Flt-I and KDR) in the endometrium and placenta of the mare during the oestrous cycle and pregnancy.. Reprod Domest Anim 2007 Oct;42(5):516-26.
  48. Herrera E. Lipid metabolism in pregnancy and its consequences in the fetus and newborn.. Endocrine 2002 Oct;19(1):43-55.
    doi: 10.1385/ENDO:19:1:43pubmed: 12583601google scholar: lookup
  49. Suire S, Stewart F, Beauchamp J, Kennedy MW. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: fatty acid and retinol binding properties, and structural characterization.. Biochem J 2001 Jun 1;356(Pt 2):369-76.
    doi: 10.1042/bj3560369pmc: PMC1221847pubmed: 11368763google scholar: lookup
  50. Bourdiec A, Ahmad SF, Lachhab A, Akoum A. Regulation of inflammatory and angiogenesis mediators in a functional model of decidualized endometrial stromal cells.. Reprod Biomed Online 2016 Jan;32(1):85-95.
    doi: 10.1016/j.rbmo.2015.09.011pubmed: 26602943google scholar: lookup
  51. Vonnahme KA, Fernando SC, Ross JW, Ashworth MD, DeSilva U, Malayer JR, Geisert RD. Porcine endometrial expression of kininogen, factor XII, and plasma kallikrein in cyclic and pregnant gilts.. Biol Reprod 2004 Jan;70(1):132-8.
    doi: 10.1095/biolreprod.103.020412pubmed: 13679312google scholar: lookup
  52. Golias Ch, Charalabopoulos A, Stagikas D, Charalabopoulos K, Batistatou A. The kinin system--bradykinin: biological effects and clinical implications. Multiple role of the kinin system--bradykinin.. Hippokratia 2007 Jul;11(3):124-8.
    pmc: PMC2658795pubmed: 19582206
  53. Hillmeister P, Persson PB. The Kallikrein-Kinin system.. Acta Physiol (Oxf) 2012 Dec;206(4):215-9.
    doi: 10.1111/apha.12007pubmed: 23110467google scholar: lookup
  54. Allen MR, Zhang BR, Hettinger AM, Goad DW, Malayer JR, Geisert RD. Detection of bradykinin and bradykinin-beta(2) receptors in the porcine endometrium during the estrous cycle and early pregnancy.. Biol Reprod 2002 Mar;66(3):574-9.
    doi: 10.1095/biolreprod66.3.574pubmed: 11870060google scholar: lookup
  55. Kawato H, Tabata T, Minoura H, Murabayashi N, Ma N, Wang DF, Sagawa N. Factor XII gene expression in endometrial stromal cells during decidualisation.. Reprod Fertil Dev 2009;21(7):840-7.
    doi: 10.1071/RD08301pubmed: 19698288google scholar: lookup
  56. Ullah K, Rahman TU, Pan HT, Guo MX, Dong XY, Liu J, Jin LY, Cheng Y, Ke ZH, Ren J, Lin XH, Qiu XX, Wang TT, Huang HF, Sheng JZ. Serum estradiol levels in controlled ovarian stimulation directly affect the endometrium.. J Mol Endocrinol 2017 Aug;59(2):105-119.
    doi: 10.1530/JME-17-0036pmc: PMC5510595pubmed: 28539318google scholar: lookup
  57. Erices R, Corthorn J, Lisboa F, Valdés G. Bradykinin promotes migration and invasion of human immortalized trophoblasts.. Reprod Biol Endocrinol 2011 Jul 5;9:97.
    doi: 10.1186/1477-7827-9-97pmc: PMC3141650pubmed: 21729302google scholar: lookup
  58. Stout TA, Allen WR. Role of prostaglandins in intrauterine migration of the equine conceptus.. Reproduction 2001 May;121(5):771-5.
    doi: 10.1530/rep.0.1210771pubmed: 11427165google scholar: lookup
  59. Morrissey NK, Bellenger CR, Baird AW. Bradykinin stimulates prostaglandin E2 production and cyclooxygenase activity in equine nonglandular and glandular gastric mucosa in vitro.. Equine Vet J 2008 Jun;40(4):332-6.
    doi: 10.2746/042516408X293556pubmed: 18331972google scholar: lookup
  60. Yoshimura Y, Espey L, Hosoi Y, Adachi T, Atlas SJ, Ghodgaonkar RB, Dubin NH, Wallach EE. The effects of bradykinin on ovulation and prostaglandin production by the perfused rabbit ovary.. Endocrinology 1988 Jun;122(6):2540-6.
    doi: 10.1210/endo-122-6-2540pubmed: 3163547google scholar: lookup
  61. Hellberg P, Larson L, Olofsson J, Hedin L, Brännström M. Stimulatory effects of bradykinin on the ovulatory process in the in vitro-perfused rat ovary.. Biol Reprod 1991 Feb;44(2):269-74.
    doi: 10.1095/biolreprod44.2.269pubmed: 2009329google scholar: lookup
  62. Nie M, Pang L, Inoue H, Knox AJ. Transcriptional regulation of cyclooxygenase 2 by bradykinin and interleukin-1beta in human airway smooth muscle cells: involvement of different promoter elements, transcription factors, and histone h4 acetylation.. Mol Cell Biol 2003 Dec;23(24):9233-44.
  63. Bradbury DA, Newton R, Zhu YM, El-Haroun H, Corbett L, Knox AJ. Cyclooxygenase-2 induction by bradykinin in human pulmonary artery smooth muscle cells is mediated by the cyclic AMP response element through a novel autocrine loop involving endogenous prostaglandin E2, E-prostanoid 2 (EP2), and EP4 receptors.. J Biol Chem 2003 Dec 12;278(50):49954-64.
    doi: 10.1074/jbc.M307964200pubmed: 14517215google scholar: lookup
  64. Dorniak P, Bazer FW, Wu G, Spencer TE. Conceptus-derived prostaglandins regulate endometrial function in sheep.. Biol Reprod 2012 Jul;87(1):9, 1-7.
    pubmed: 22517622doi: 10.1095/biolreprod.112.100487google scholar: lookup
  65. Simmons RM, Erikson DW, Kim J, Burghardt RC, Bazer FW, Johnson GA, Spencer TE. Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation.. Endocrinology 2009 Sep;150(9):4295-305.
    doi: 10.1210/en.2009-0060pubmed: 19497977google scholar: lookup
  66. Robinson RS, Mann GE, Gadd TS, Lamming GE, Wathes DC. The expression of the IGF system in the bovine uterus throughout the oestrous cycle and early pregnancy.. J Endocrinol 2000 May;165(2):231-43.
    doi: 10.1677/joe.0.1650231pubmed: 10810287google scholar: lookup
  67. Herrler A, Pell JM, Allen WR, Beier HM, Stewart F. Horse conceptuses secrete insulin-like growth factor-binding protein 3.. Biol Reprod 2000 Jun;62(6):1804-11.
    doi: 10.1095/biolreprod62.6.1804pubmed: 10819785google scholar: lookup
  68. Walters KW, Roser JF, Anderson GB. Maternal-conceptus signalling during early pregnancy in mares: oestrogen and insulin-like growth factor I.. Reproduction 2001 Feb;121(2):331-8.
    doi: 10.1530/rep.0.1210331pubmed: 11226058google scholar: lookup
  69. Forbes K, Souquet B, Garside R, Aplin JD, Westwood M. Transforming growth factor-{beta} (TGF{beta}) receptors I/II differentially regulate TGF{beta}1 and IGF-binding protein-3 mitogenic effects in the human placenta.. Endocrinology 2010 Apr;151(4):1723-31.
    doi: 10.1210/en.2009-0896pubmed: 20172969google scholar: lookup
  70. Baxter RC. Insulin-like growth factor binding protein-3 (IGFBP-3): Novel ligands mediate unexpected functions.. J Cell Commun Signal 2013 Aug;7(3):179-89.
    doi: 10.1007/s12079-013-0203-9pmc: PMC3709052pubmed: 23700234google scholar: lookup
  71. Li Y, Fong KW, Tang M, Han X, Gong Z, Ma W, Hebert M, Songyang Z, Chen J. Fam118B, a newly identified component of Cajal bodies, is required for Cajal body formation, snRNP biogenesis and cell viability.. J Cell Sci 2014 May 1;127(Pt 9):2029-39.
    doi: 10.1242/jcs.143453pmc: PMC4004977pubmed: 24569877google scholar: lookup
  72. de Ruijter-Villani M, van Boxtel PR, Stout TA. Fibroblast growth factor-2 expression in the preimplantation equine conceptus and endometrium of pregnant and cyclic mares.. Theriogenology 2013 Dec;80(9):979-89.
  73. Stout TA. Equine embryo transfer: review of developing potential.. Equine Vet J 2006 Sep;38(5):467-78.
    doi: 10.2746/042516406778400529pubmed: 16986609google scholar: lookup
  74. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. Galaxy: a web-based genome analysis tool for experimentalists.. Curr Protoc Mol Biol 2010 Jan;Chapter 19:Unit 19.10.1-21.
  75. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.. Genome Biol 2013 Apr 25;14(4):R36.
    doi: 10.1186/gb-2013-14-4-r36pmc: PMC4053844pubmed: 23618408google scholar: lookup
  76. Gaidatzis D, Lerch A, Hahne F, Stadler MB. QuasR: quantification and annotation of short reads in R.. Bioinformatics 2015 Apr 1;31(7):1130-2.
  77. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  78. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.. Nat Protoc 2009;4(1):44-57.
    doi: 10.1038/nprot.2008.211pubmed: 19131956google scholar: lookup
  79. de Grauw JC, van de Lest CH, van Weeren PR. A targeted lipidomics approach to the study of eicosanoid release in synovial joints.. Arthritis Res Ther 2011 Jul 27;13(4):R123.
    doi: 10.1186/ar3427pmc: PMC3239362pubmed: 21794148google scholar: lookup
  80. Cokelaere SM, Plomp SGM, de Boef E, de Leeuw M, Bool S, van de Lest CHA, van Weeren PR, Korthagen NM. Sustained intra-articular release of celecoxib in an equine repeated LPS synovitis model.. Eur J Pharm Biopharm 2018 Jul;128:327-336.
    doi: 10.1016/j.ejpb.2018.05.001pubmed: 29729412google scholar: lookup

Citations

This article has been cited 3 times.
  1. Gibson C, de Ruijter-Villani M, Stout TAE. Insulin-like growth factor system components expressed at the conceptus-maternal interface during the establishment of equine pregnancy.. Front Vet Sci 2022;9:912721.
    doi: 10.3389/fvets.2022.912721pubmed: 36176700google scholar: lookup
  2. Shen Y, Ren H, Davshilt T, Tian S, Wang X, Yi M, Ulaangerel T, Li B, Dugarjav M, Bou G. The transcriptome landscapes of allantochorion and vitelline-chorion in equine day 30 conceptus.. Front Cell Dev Biol 2022;10:958205.
    doi: 10.3389/fcell.2022.958205pubmed: 35990610google scholar: lookup
  3. Bauersachs S, Almiñana C. Embryo-Maternal Interactions Underlying Reproduction in Mammals.. Int J Mol Sci 2020 Jul 10;21(14).
    doi: 10.3390/ijms21144872pubmed: 32664189google scholar: lookup