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Progesterone Supplementation During the Pre-implantation Period Influences Interferon-Stimulated Gene Expression in Lactating Dairy Cows Cover

Progesterone Supplementation During the Pre-implantation Period Influences Interferon-Stimulated Gene Expression in Lactating Dairy Cows

Open Access
|Jul 2019

References

  1. Alhussien M.N., Kamboj A., Aljader M.A., Panda B.S.K., Yadav M.L., Sharma L., Mohammed S., Sheikh A.A., Lotfan M., Kapila R., Mohanty A.K., Dang A.K. (2018). Effect of tropical thermal stress on peri-implantation immune responses in cows. Theriogenology, 114: 149–15810.1016/j.theriogenology.2018.03.036
  2. Ayalon N. (1978). A review of embryonic mortality in cattle. J. Reprod. Fertil., 54: 483–493.10.1530/jrf.0.0540483
  3. Binelli M., Subramaniam P., Diaz T., Johnson G.A., Hansen T.R., Badinga L., Thatcher W.W. (2001). Bovine interferon-tau stimulates the Janus kinase-signal transducer and activator of transcription pathway in bovine endometrial epithelial cells. Biol. Reprod., 64: 654–665.10.1095/biolreprod64.2.654
  4. Bridges G.A., Day M.L., Geary T.W., Cruppe L.H. (2013). Triennial Reproduction Symposium: deficiencies in the uterine environment and failure to support embryonic development. J. Anim. Sci., 91: 3002–3013.10.2527/jas.2013-5882
  5. Carter F., Forde N., Duffy P., Wade M., Fair T., Crowe M.A., Evans A.C., Kenny D.A., Roche J.F., Lonergan P. (2008). Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod. Fert. Develop., 20: 368–375.10.1071/RD07204
  6. Chomczynski P., Sacchi N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal. Biochem., 162: 156–159.10.1016/0003-2697(87)90021-2
  7. Clemente M., de La Fuente J., Fair T., Al Naib A., Gutierrez-Adan A., Roche J. F., Rizos D., Lonergan P. (2009). Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction, 138: 507–517.10.1530/REP-09-0152
  8. Committee on Bovine Reproductive Nomenclature (1972). Recommendations for standardizing bovine reproductive terms. Cornell Vet., 62: 216–237.
  9. Forde N., Carter F., Fair T., Crowe M.A., Evans A.C., Spencer T.E., Bazer F.W., Mc-Bride R., Boland M.P., O ’ Gaora P., Lonergan P., Roche J.F. (2009). Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol. Reprod., 81: 784–794.10.1095/biolreprod.108.074336
  10. Forde N., Spencer T.E., Bazer F.W., Song G., Roche J.F., Lonergan P. (2010). Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol. Genomics, 41: 53–62.10.1152/physiolgenomics.00162.2009
  11. Forde N., Duffy G.B., McGettigan P.A., Browne J.A., Mehta J.P., Kelly A.K., Mansouri-Attia N., Sandra O., Loftus B.J., Crowe M.A., Fair T., Roche J.F., Lonergan P., Evans A.C. (2012). Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiol. Genomics, 44: 799–810.10.1152/physiolgenomics.00067.2012
  12. Friedman E., Roth Z., Voet H., Lavon Y., Wolfenson D. (2012). Progesterone supplementation postinsemination improves fertility of cooled dairy cows during the summer. J. Dairy Sci., 95: 3092–3099.10.3168/jds.2011-5017
  13. García-Ispierto I., López-Gatius F. (2012). Effects of GnRH or progesterone treatment on day 5 post-AI on plasma progesterone, luteal blood flow and leucocyte counts during the luteal phase in dairy cows. Reprod. Domest. Anim., 47: 224–229.10.1111/j.1439-0531.2011.01832.x
  14. García-Ispierto I., López-Gatius F. (2014). Effects of different five-day progesterone-based fixed-time AI protocols on follicular/luteal dynamics and fertility in dairy cows. J. Reprod. Dev., 60: 426–432.10.1262/jrd.2014-063
  15. García-Ispierto I., López-Gatius F. (2017). Progesterone supplementation in the early luteal phase after artificial insemination improves conception rates in high-producing dairy cows. Theriogenology, 90: 20–24.10.1016/j.theriogenology.2016.11.006
  16. García-Ispierto I., López-Helguera I., Serrano-Pérez B., Paso V., Tuono T., Ramon A., Mur-Novales R., Tutusaus J., López-Gatius F. (2016). Progesterone supplementation during the time of pregnancy recognition after artificial insemination improves conception rates in high-producing dairy cows. Theriogenology, 85: 1343–1347.10.1016/j.theriogenology.2015.12.021
  17. Garrett J.E., Geisert R.D., Zavy M.T., Morgan G.L. (1988). Evidence for maternal regulation of early conceptus growth and development in beef cattle. J. Reprod. Fertil., 84: 437–446.10.1530/jrf.0.0840437
  18. Gifford C.A., Racicot K., Clark D.S., Austin K.J., Hansen T.R., Lucy M.C., Davies C.J., Ott T.L. (2007). Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. J. Dairy Sci., 90: 274–280.10.3168/jds.S0022-0302(07)72628-0
  19. Green J.C., Okamura C.S., Poock S.E., Lucy M.C. (2010). Measurement of interferon-tau (IFN-tau) stimulated gene expression in blood leukocytes for pregnancy diagnosis within 18–20d after insemination in dairy cattle. Anim. Reprod. Sci., 121: 24–33.10.1016/j.anireprosci.2010.05.010
  20. Guillomot M., Fléchon J.E., Leroy F. (1993). Blastocyst development and implantation. In: Reproduction in mammals and man, Thibault C., Levasseur M.C., Hunter R.H.F. (eds). Paris, Ellipses, pp. 387–410.
  21. Han H., Austin K.J., Rempel L.A., Hansen T.R. (2006). Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. J. Endocrinol., 191: 505–512.10.1677/joe.1.07015
  22. Hansen P.J. (2007). Hidden factors affecting fertility. WCDS Advances in Dairy Technology 19: 339–349.
  23. King G.J., Atkinson B.A., Robertson H.A. (1980). Development of the bovine placentome from days 20 to 29 of gestation. J. Reprod. Fertil., 59: 95–100.10.1530/jrf.0.0590095
  24. King G.J., Atkinson B.A., Robertson H.A. (1981). Development of the intercaruncular areas during early gestation and establishment of the bovine placenta. J. Reprod. Fertil., 61: 469–474.10.1530/jrf.0.0610469
  25. Klein C., Bauersachs S., Ulbrich S.E., Einspanier R., Meyer H.H., Schmidt S.E., Reichenbach H.D., Vermehren M., Sinowatz F., Blum H., Wolf E. (2006). Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the preattachment period. Biol. Reprod., 74: 253–264.10.1095/biolreprod.105.046748
  26. Kose M., Kaya M.S., Aydilek N., Kucukaslan I., Bayril T., Bademkiran S., Kima Z., Ozyurtlu N., Kayis S.A., Guzeloglu A., Atli M.O. (2016). Expression profile of interferon tau-stimulated genes in ovine peripheral blood leukocytes during embryonic death. Theriogenology, 85: 1161–1166.10.1016/j.theriogenology.2015.11.032
  27. Lonergan P., Forde N., Spencer T.E. (2016). Role of progesterone in embryo development in cattle. Reprod. Fertil. Dev., 28: 66–74.10.1071/RD15326
  28. López-Gatius F. (2003). Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology, 60: 89–99.10.1016/S0093-691X(02)01359-6
  29. López-Gatius F. (2012). Factors of a noninfectious nature affecting fertility after artificial insemination in lactating dairy cows. A review. Theriogenology, 77: 1029–1041.10.1016/j.theriogenology.2011.10.014
  30. López-Gatius F., García-Ispierto I. (2010). Ultrasound and endocrine findings that help to assess the risk of late embryo/early foetal loss by non-infectious cause in dairy cattle. Reprod. Domest. Anim., 45: 15–24.10.1111/j.1439-0531.2010.01620.x
  31. López-Gatius F., Hunter R.H.F. (2017). From pre-ovulatory follicle palpation to the challenge of twin pregnancies: Clinical reflections following one million gynaecological examinations in dairy cows. Reprod. Domest. Anim., 52: 4–11.10.1111/rda.13041
  32. López-Gatius F., Labèrnia J., Santolaria P., López-Béjar M., Rutllant J. (1996). Effect of reproductive disorders previous to conception on pregnancy attrition in dairy cows, Theriogenology, 46: 643–648.10.1016/0093-691X(96)00215-4
  33. López-Gatius F., García-Ispierto I., Santolaria P., Yániz J., Nogareda C., López-Béjar M. (2006). Screening for high fertility in high-producing dairy cows. Theriogenology, 65: 1678–1689.10.1016/j.theriogenology.2005.09.027
  34. López-Gatius F., Garbayo J.M., Santolaria P., Yániz J., Ayad A., de Sousa N.M., Beckers J.F. (2007). Milk production correlates negatively with plasma levels of pregnancy-associated glycoprotein (PAG) during the early foetal period in high producing dairy cows with live fetuses. Domest. Anim. Endocrinol., 32: 29–42.10.1016/j.domaniend.2005.12.007
  35. Lucy M.C. (2001). Reproductive loss in high-producing dairy cattle: where will it end? J. Dairy Sci., 84: 1277–1293.10.3168/jds.S0022-0302(01)70158-0
  36. Manjari P., Reddi S., Alhussien M., Mohammed S., De S., Mohanty A.K., Sivalingam J., Dang A.K. (2016). Neutrophil gene dynamics and plasma cytokine levels in dairy cattle during peri-implantation period. Vet. Immunol. Immunopathol., 173: 44–49.10.1016/j.vetimm.2016.03.017
  37. Mann G.E., Lamming G.E. (2001). Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction, 121: 175–180.10.1530/rep.0.1210175
  38. Mann G.E., Fray M.D., Lamming G.E. (2006). Effects of time of progesterone supplementation on embryo development and interferon-tau production in the cow. Vet J., 171: 500–503.10.1016/j.tvjl.2004.12.005
  39. Matsuyama S., Kojima T., Kato S., Kimura K. (2012). Relationship between quantity of IFNT estimated by IFN-stimulated gene expression in peripheral blood mononuclear cells and bovine embryonic mortality after AI or ET. Reprod. Biol. Endocrinol., 10: 21.10.1186/1477-7827-10-21
  40. Meyerholz M.M., Mense K., Knaack H., Sandra O., Schmicke M. (2016). Pregnancy-induced ISG-15 and MX-1 gene expression is detected in the liver of Holstein-Friesian heifers during late peri-implantation period. Reprod. Domest. Anim., 51: 175–177.10.1111/rda.12638
  41. Monteiro P.L. Jr., Ribeiro E.S., Maciel R.P., Dias A.L., Solé E. Jr., Lima F.S., Bisinotto R.S., Thatcher W.W., Sartori R., Santos J.E. (2014). Effects of supplemental progesterone after artificial insemination on expression of interferon-stimulated genes and fertility in dairy cows. J. Dairy Sci., 97: 4907–4921.10.3168/jds.2013-7802
  42. Monteiro P.L. Jr., Nascimento A.B., Pontes G.C., Fernandes G.O., Melo L.F., Wiltbank M.C., Sartori R. (2015). Progesterone supplementation after ovulation: effects on corpus luteum function and on fertility of dairy cows subjected to AI or ET. Theriogenology, 84: 1215–1224.10.1016/j.theriogenology.2015.06.023
  43. Paradis F., Yue S., Grant J.R., Stothard P., Basarab J.A., Fitzsimmons C. (2015). Transcriptomic analysis by RNA sequencing reveals that hepatic interferon-induced genes may be associated with feed efficiency in beef heifers. J. Anim. Sci., 93: 3331–3341.10.2527/jas.2015-8975
  44. Parr M.H., Crowe M.A., Lonergan P., Evans A.C., Rizos D., Diskin M.G. (2014). Effect of exogenous progesterone supplementation in the early luteal phase post-insemination on pregnancy per artificial insemination in Holstein-Friesian cows. Anim. Reprod. Sci., 150: 7–14.10.1016/j.anireprosci.2014.08.008
  45. Peter A.T., Beg M.A., Ahmad E., Bergfelt D.R. (2017). Trophoblast of domestic and companion animals: basic and applied clinical perspectives. Anim. Reprod., 14: 1209–1224.10.21451/1984-3143-AR973
  46. Pugliesi G., Miagawa B.T., Paiva Y.N., França M.R., Silva L.A., Binelli M. (2014). Conceptus-induced changes in the gene expression of blood immune cells and the ultrasound-accessed luteal function in beef cattle: how early can we detect pregnancy? Biol. Reprod., 91: 95.10.1095/biolreprod.114.121525
  47. Ribeiro E.S., Bruno R.G., Farias A.M., Hernández-Rivera J.A., Gomes G.C., Surjus R., Becker L.F., Birt A., Ott T.L, Branen J.R., Sasser R.G., Keisler D.H., Thatcher W.W., Bilby T.R., Santos J.E. (2014). Low doses of bovine somatotropin enhance conceptus development and fertility in lactating dairy cows. Biol. Reprod., 90: 10.10.1095/biolreprod.113.114694
  48. Ribeiro E.S., Gomes G., Greco L.F., Cerri R.L., Vieira-Neto A., Monteiro P.L. Jr., Lima F.S., Bisinotto R.S., Thatcher W.W., Santos J.E. (2016). Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows. J. Dairy Sci., 99: 2201–2220.10.3168/jds.2015-10337
  49. Roberts R.M., Leaman D.W., Cross J.C. (1992). Role of interferons in maternal recognition of pregnancy in ruminants. Proc. Soc. Exp. Biol. Med., 200: 7–18.10.3181/00379727-200-43387A
  50. Ruhmann B., Giller K., Hankele A.K., Ulbrich S.E., Schmicke M. (2017). Interferon-τ induced gene expression in bovine hepatocytes during early pregnancy. Theriogenology, 104: 198–204.10.1016/j.theriogenology.2017.07.051
  51. Serrano-Pérez B., Hansen P.J., Mur-Novales R., García-Ispierto I., de Sousa N.M., Beckers J.F., Almería S., López-Gatius F. (2016). Crosstalk between uterine serpin (SERPINA14) and pregnancy-associated glycoproteins at the foetal-maternal interface in pregnant dairy heifers experimentally infected with Neospora caninum. Theriogenology, 86: 824–830.10.1016/j.theriogenology.2016.03.003
  52. Shirasuna K., Matsumoto H., Kobayashi E., Nitta A., Haneda S., Matsui M., Kawashima C., Kida K., Shimizu T., Miyamoto A. (2012). Upregulation of interferon-stimulated genes and interleukin-10 in peripheral blood immune cells during early pregnancy in dairy cows. J. Reprod. Dev., 58: 84–90.10.1262/jrd.11-094K
  53. Spencer T.E., Johnson G.A., Bazer F.W., Burghardt R.C., Palmarini M. (2007). Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod. Fert. Develop., 19: 65–78.10.1071/RD06102
  54. Spencer T.E., 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: 5941–5950.10.3168/jds.2015-10070
  55. Stevenson J.S., Portaluppi M.A., Tenhouse D.E., Lloyd A., Eborn D.R., Kacuba S., De Jarnette J.M. (2007). Interventions after artificial insemination: conception rates, pregnancy survival, and ovarian responses to gonadotropin-releasing hormone, human chorionic gonadotropin, and progesterone. J. Dairy Sci., 90: 331–340.10.3168/jds.S0022-0302(07)72634-6
  56. Wijma R., Stangaferro M.L., Kamat M.M., Vasudevan S., Ott T.L., Giordano J.O. (2016). Embryo mortality around the period of maintenance of the corpus luteum causes alterations to the ovarian function of lactating dairy cows. Biol. Reprod., 95: 112.10.1095/biolreprod.116.142075
  57. Yan L., Robinson R., Shi Z., Mann G. (2016). Efficacy of progesterone supplementation during early pregnancy in cows: a meta-analysis. Theriogenology, 85: 1390–1398.10.1016/j.theriogenology.2015.12.027
  58. Yuan J.S., Reed A., Chen F., Stewart C.N. Jr. (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics, 7: 85.10.1186/1471-2105-7-85
DOI: https://doi.org/10.2478/aoas-2019-0019 | Journal eISSN: 2300-8733 | Journal ISSN: 1642-3402
Language: English
Page range: 713 - 724
Submitted on: Oct 12, 2018
Accepted on: Feb 20, 2019
Published on: Jul 30, 2019
Published by: National Research Institute of Animal Production
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2019 Beatriz Serrano-Pérez, Dimitrios Rizos, Irene López-Helguera, Ester Molina, Irina Garcia-Ispierto, Fernando López-Gatius, published by National Research Institute of Animal Production
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.