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Roles of Conceptus Secretory Proteins in Establishment and Maintenance of Pregnancy in Ruminants

  • Bazer, Fuller W. (Department of Animal Science and Center for Animal Biotechnology and Genomics, Texas A&M University) ;
  • Song, Gwon-Hwa (WCU Biomodulation, Department of Agricultural Biotechnology, Seoul National University) ;
  • Thatcher, William W. (Department of Animal Sciences, University of Florida)
  • 발행 : 2012.01.01

초록

Reproduction in ruminant species is a highly complex biological process requiring a dialogue between the developing conceptus (embryo-fetus and associated placental membranes) and maternal uterus which must be established during the peri-implantation period for pregnancy recognition signaling and regulation of gene expression by uterine epithelial and stromal cells. The uterus provide a microenvironment in which molecules secreted by uterine epithelia and transported into the uterine lumen represent histotroph, also known as the secretome, that are required for growth and development of the conceptus and receptivity of the uterus to implantation by the elongating conceptus. Pregnancy recognition signaling as related to sustaining the functional lifespan of the corpora lutea, is required to sustain the functional life-span of corpora lutea for production of progesterone which is essential for uterine functions supportive of implantation and placentation required for successful outcomes of pregnancy. It is within the peri-implantation period that most embryonic deaths occur in ruminants due to deficiencies attributed to uterine functions or failure of the conceptus to develop appropriately, signal pregnancy recognition and/or undergo implantation and placentation. The endocrine status of the pregnant ruminant and her nutritional status are critical for successful establishment and maintenance of pregnancy. The challenge is to understand the complexity of key mechanisms that are characteristic of successful reproduction in humans and animals and to use that knowledge to enhance fertility and reproductive health of ruminant species in livestock enterprises.

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참고문헌

  1. Anthony, R. V., S. L. Pratt, R. Liang and M. D. Holland. 1995. Placental-fetal hormonal interactions: Impact on fetal growth. J. Anim. Sci. 73:1861-1871.
  2. Ashworth, C. J. and F. W. Bazer. 1989. Interrelationships of proteins secreted by the ovine conceptus and endometrium during the preiattachment period. Anim. Reprod. Sci. 20:117-130. https://doi.org/10.1016/0378-4320(89)90069-9
  3. Barros, C. M., J. G. Betts, W. W. Thatcher and P. J. Hansen. 1992. Possible mechanisms for reduction of circulating concentra-tions of progesterone by interferon-$\alpha$ in cows: Effects on hyperthermia, luteal cells, metabolism of progesterone and secretion of LH. J. Endocrinol. 133:175-182. https://doi.org/10.1677/joe.0.1330175
  4. Bazer, F. W. and N. L. First. 1983. Pregnancy and parturition. J. Anim. Sci. 57(Suppl. 2):425-458.
  5. Bazer, F. W., T. L. Ott and T. E. Spencer. 1994. Pregnancy recognition in ruminants, pigs and horses: signals from the trophoblast. Theriogenology 41:79-94. https://doi.org/10.1016/S0093-691X(05)80052-4
  6. Bazer, F. W., T. E. Spencer and G. A. Johnson. 2009. Interferons and uterine receptivity. Semin. Reprod. Med. 27:90-102. https://doi.org/10.1055/s-0028-1108013
  7. Bazer, F. W., G. Wu, T. E. Spencer, G. A. Johnson, R. C. Burghardt and K. Bayless. 2010. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol. Hum. Reprod. 16:135-152. https://doi.org/10.1093/molehr/gap095
  8. Bazer, F. W., T. E. Spencer, G. A. Johnson and R. C. Burghardt. 2011a. Uterine receptivity to implantation of blastocysts in mammals. Front. Biosci. S3:745-767.
  9. Bazer, F. W., G. Wu, G. A. Johnson, J. Kim and G. Song. 2011b. Uterine histotroph and conceptus development: Select nutrients and secreted phosphoprotein 1 affect MTOR cell signaling in ewes. Biol. Reprod. Aug 24. (Epub ahead of print).
  10. Bott, R. C., R. L. Ashley, L. E. Henkes, A. Q. Antoniazzi, J. E. Bruemmer, G. D. Niswender, F. W. Bazer, T. E. Spencer, N. P. Smirnova, R. V. Anthony and T. R. Hansen. 2010. Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes. Biol. Reprod. 82:725-735. https://doi.org/10.1095/biolreprod.109.079467
  11. Carson, D. D., E. Lagow, A. Thathiah, R. Al-Shami, M. C. Farach-Carson, M. Vernon, L. Yuan, M. A. Fritz and B. Lessey. 2002. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol. Hum. Reprod. 8:871-879. https://doi.org/10.1093/molehr/8.9.871
  12. Chami, O., A. Megevand, T. L. Ott, F. W. Bazer and C. O'Neill. 1999. A role for platelet-activating factor as an endogenous pulse-generator for the release of luteolytic PGF from the ovine endometrium. Am. J. Physiol. 276:E783-E792.
  13. Charleston, B. and H. J. Stewart. 1993. An interferon-induced Mx protein: cDNA sequence and high level expression in the endometrium of pregnant sheep. Gene 137:327-331. https://doi.org/10.1016/0378-1119(93)90029-3
  14. Chen, C., T. E. Spencer and F. W. Bazer. 2000a. Fibroblast growth factor-10: A stromal mediator of epithelial function in the ovine uterus. Biol. Reprod. 63:959-966. https://doi.org/10.1095/biolreprod63.3.959
  15. Chen, C., T. E. Spencer and F. W. Bazer. 2000b. Expression of hepatocyte growth factor and its receptor c-met in the ovine uterus. Biol. Reprod. 62:1844-1850. https://doi.org/10.1095/biolreprod62.6.1844
  16. Chen, E. Y., Y. C. Liao, D. H. Smith, H. A. Barrera-Saldana, R. E. Gelinas and P. H. Seeburg. 1989. The human growth hormone locus nucleotide sequence, biology and evolution. Genomics 4:479-497. https://doi.org/10.1016/0888-7543(89)90271-1
  17. Chilton, B. S. and J. C. Daniel. 1987. Differences in the rabbit uterine response to progesterone as influenced by growth hormone or prolactin. J. Reprod. Fertil. 79:581-587. https://doi.org/10.1530/jrf.0.0790581
  18. Chilton, B. S., S. K. Mani and D. W. Bullock. 1988. Servomechanism of prolactin and progesterone in regulating uterine gene expression. Mol. Cell. Endocrinol. 2:1169-1175. https://doi.org/10.1210/mend-2-12-1169
  19. Cooke, F. N., K. A. Pennington, Q. Yang and A. D. Ealy. 2009. Several fibroblast growth factors are expressed during pre-attachment bovine conceptus development and regulate interferon-tau expression from trophectoderm. Reproduction 137:259-269. https://doi.org/10.1530/REP-08-0396
  20. Danet-Desnoyers, G., C. Wetzels and W. W. Thatcher. 1994. Natural and recombinant bovine interferon tau regulate basal and oxytocin-induced secretion of prostaglandins F2 alpha and E2 by epithelial cells and stromal cells in the endometrium. Reprod. Fertil. Dev. 6:193-202. https://doi.org/10.1071/RD9940193
  21. Darnell, J. E. Jr., I. M. Kerr and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Sciences 264:1415-1421. https://doi.org/10.1126/science.8197455
  22. Davis, M. A., T. L. Ott, M. A. Mirando, M. T. Moser and F. W. Bazer. 1992. Effect of recombinant alpha interferons on fertility and interstrous interval in sheep. Theriogenology 38:867-875. https://doi.org/10.1016/0093-691X(92)90162-K
  23. Dorniak, P., F. W. Bazer and T. E. Spencer. 2011. Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol. Reprod. 84:1119-1127. https://doi.org/10.1095/biolreprod.110.089979
  24. Drost, M., J. M. Wright and R. P. Elsden. 1986. Intergeneric embryo transfer between water buffalo and domestic cattle. Theriogenology 25:13-23. https://doi.org/10.1016/0093-691X(86)90180-9
  25. Eley, R. M., W. W. Thatcher, F. W. Bazer and M. J. Fields. 1983. Steroid metabolism by the bovine uterine endometrium and conceptus. Biol. Reprod. 28:804-816. https://doi.org/10.1095/biolreprod28.4.804
  26. Fincher, K. B., F. W. Bazer, P. J. Hansen, W. W. Thatcher and R. M. Roberts. 1986. Proteins secreted by the sheep conceptus suppress induction of uterine prostaglandin F2a release by estradiol and oxytocin. J. Reprod. Fertil. 76:425-433. https://doi.org/10.1530/jrf.0.0760425
  27. Fleming, J. G. W., T. E. Spencer, S. H. Safe and F. W. Bazer. 2006. The ovine uterine oxytocin receptor gene: Regulation of expression by estradiol and role of IFNT signaling for establishment of pregnancy in ruminants. Endocrinology 147:899-911. https://doi.org/10.1210/en.2005-1120
  28. Fliss, A. E., F. J. Michel, C. L. Chen, F. W. Hofig, J. Y. Chou and R. C. M. Simmen. 1991. Regulation of the uteroferrin gene promoter in endometrial cells: Interactions between estrogen, progesterone and prolactin. Endocrinology 129:697-704. https://doi.org/10.1210/endo-129-2-697
  29. Freemark, M. and M. Comer. 1989. Purification of a distinct placental lactogen receptor, a new member of the growth hormone/prolactin family. J. Clin. Invest. 83:883-889. https://doi.org/10.1172/JCI113972
  30. Galosy, S., A. Gertler, G. Elberg and D. Laird. 1991. Distinct placental lactogen and prolactin (lactogen) receptors in bovine endometrium. Mol. Cell. Endocrinol. 78:229-236. https://doi.org/10.1016/0303-7207(91)90127-E
  31. Gootwine, E., J. A. Sise, J. M. Penty and G. W. Montgomery. 1993. The duplicated gene copy of the ovine growth hormone gene contain a Pvu II polymorphism in the second intron. Anim. Genet. 24:319-321.
  32. Guillomot, M. 1995. Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 49:39-51.
  33. Han, H., K. J. Austin, L. A. Rempel and T. R. Hansen. 2006. Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. J. Endocrinol. 191:505-512. https://doi.org/10.1677/joe.1.07015
  34. Helmer, S. D., T. S. Gross, G. R. Newton, P. J. Hansen and W. W. Thatcher. 1989. Bovine trophoblast protein-1 complex alters endometrial protein and prostaglandin secretion and induces an intracellular inhibitor of prostaglandin synthesis in vitro. J. Reprod. Fertil. 87:421-430. https://doi.org/10.1530/jrf.0.0870421
  35. Hernandez-Ledezma, J. J., J. D. Sikes, C. N. Murphy, A. J. Watson, G. A. Schultz and R. M. Roberts. 1992. Expression of bovine trophoblast interferon in conceptuses derived by in vitro techniques. Biol. Reprod. 47:374-380. https://doi.org/10.1095/biolreprod47.3.374
  36. Imakawa, K., S. D. Helmer, K. P. Nephew, C. S. R. Meka and R. K. Christenson. 1993. A novel role for GM-CSF: Enhancement of pregnancy specific interferon production, ovine trophoblast protein-1. Endocrinology 132:1869-1871. https://doi.org/10.1210/en.132.4.1869
  37. Ismail, S. T. 1987. Reproduction in the female camel (Camelus dromedarius). Theriogenology 28:363-371. https://doi.org/10.1016/0093-691X(87)90024-0
  38. Ing, N. H. and R. M. Roberts. 1989. The major progesterone-modulated proteins secreted into the sheep uterus are members of the serpin superfamily of serine protease inhibitors. J. Biol. Chem. 264:3372-3379.
  39. Kim, J., R. C. Burghardt, G. Wu, G. A. Johnson, T. E. Spencer and F. W. Bazer. 2011a. Select Nutrients in the ovine uterine lumen: VII. Effects of arginine, leucine, glutamine and glucose on trophectodem cell signaling, proliferation and migration. Biol. Reprod. 84:70-78. https://doi.org/10.1095/biolreprod.110.085753
  40. Kim, J., R. C. Burghardt, G. Wu, G. A. Johnson, T. E. Spencer and F. W. Bazer. 2011b. Select Nutrients in the ovine uterine lumen: VIII. Arginine stimulates proliferation of ovine trophectoderm cells through mTOR-RPS6K-RPS6 signaling cascade and synthesis of nitric oxide and polyamines. Biol. Reprod. 84:62-69. https://doi.org/10.1095/biolreprod.110.085738
  41. Knickerbocker, J. J., W. W. Thatcher, F. W. Bazer, M. Drost, D. H. Barron, K. B. Fincher and R. M. Roberts. 1986a. Proteins secreted by day-16 to -18 bovine conceptuses extend corpus luteum function in cows. J. Reprod. Fertil. 77:381-391. https://doi.org/10.1530/jrf.0.0770381
  42. Knickerbocker, J. J., W. W. Thatcher, F. W. Bazer, D. H. Barron and R. M. Roberts. 1986b. Inhibition of uterine prostaglandin-F2 alpha production by bovine conceptus secretory proteins. Prostaglandins 31:777-793. https://doi.org/10.1016/0090-6980(86)90180-2
  43. Lacroix, M. C., J. Guibourdenche, J. L. Frendo, G. Pidoux and D. Evain-Brion. 2002. Placental growth hormones. Endocrine 19:73-79. https://doi.org/10.1385/ENDO:19:1:73
  44. Lee, J. S. and W. J. Silvia. 1994. Cellular mechanisms mediating the stimulation of ovine endometrial secretion of prostaglandin $F_{2{\alpha}}$ in response to oxytocin: role of phospholipase $A_2$. J. Endocrinol. 141:491-496. https://doi.org/10.1677/joe.0.1410491
  45. Loureiro, B., J. Block, M. G. Favoreto, S. Carambula, K. A. Pennington, A. D. Ealy and P. J. Hansen. 2011. Consequences of conceptus exposure to colony-stimulating factor 2 on survival, elongation, interferon-τsecretion, and gene expression. Reproduction 141:617-624. https://doi.org/10.1530/REP-10-0511
  46. McCracken, J. A., W. Schramm and W. C. Okulicz. 1984. Hormone receptor control of pulsatile secretion of $PGF_{2{\alpha}}$ from ovine uterus during luteolysis and its abrogation in early pregnancy. Anim. Reprod. Sci. 7:31-56. https://doi.org/10.1016/0378-4320(84)90027-7
  47. McCracken, J. A., E. E. Custer and J. C. Lamsa. 1999. Luteolysis: A neuroendocrine-mediated event. Physiol. Rev. 79:263-323.
  48. Meyer, M. D., M. Drost, T. L. Ott, F. W. Bazer, L. Badinga, J. Li, R. M. Roberts, P. J. Hansen and W. W. Thatcher. 1995. Recombinant bovine and ovine interferon tau extend CL lifespan and reduce uterine secretion of prostaglandin $F_{2{\alpha}}$ in cattle. J. Dairy Sci. 78:1921-1931. https://doi.org/10.3168/jds.S0022-0302(95)76817-5
  49. Mishra, D. P., H. H. Meyer and B. S. Prakash. 2003. Validation of a sensitive enzyme immunoassay for 13,14-dihydro-15-keto-PGF2 alpha in buffalo plasma and its application for reproductive health status monitoring. Anim. Reprod. Sci. 15:78:33-46. https://doi.org/10.1016/S0378-4320(03)00047-2
  50. Morton, H. 1985. EPF as a pregnancy protein. In: Early Pregnancy Factor (Ed. F. Ellendorf and E. Koch). Perinatology Press, Ithaca, New York, pp. 53-64.
  51. Nephew, K. P., K. E. McClure, M. L. Day, S. Xie, R. M. Roberts and W. F. Pope. 1990. Effects of intramuscular administration of recombinant bovine interferon-$alpha_I1$ during the period of maternal recognition of pregnancy. J. Anim. Sci. 68:2766-2770.
  52. Noel, S., A. Herman, C. A. Johnson, C. A. Gray, M. D. Stewart, F. W. Bazer, A. Gertler and T. E. Spencer. 2003. Ovine placental lactogen specifically binds to endometrial glands of the ovine uterus. Biol. Reprod. 68:772-780.
  53. O'Neill, C., X. Wells and K. Battye. 1990. Embryo-derived platelet activating factor: Interactions with the arachidonic acid cascade and the establishment and maintenance of pregnancy. Reprod. Fertil. Dev. 2:423-441. https://doi.org/10.1071/RD9900423
  54. Ott, T. L., A. A. Wiley, T. E. Spencer, F. F. Bartol and F. W. Bazer. 1995. Uterine expression of interferon-induced Mx in cyclic and pregnant ewes. Biol. Reprod. 52 (Suppl 1):143(Abstr.).
  55. Ott, T. L., J. C. W. Fleming, T. E Spencer, M. M. Joyce, P. Chen, C. N. K. Green, D. Zhu, T. H. Welsh, P. G. Harms and F. W. Bazer. 1997. Effect of exogenous recombinant ovine interferon tau on circulating concentrations of progesterone, cortisol, LH and antiviral activity, interestrous interval, rectal temperature, and uterine response to oxytocin in cyclic ewes. Biol. Reprod. 57:621-629. https://doi.org/10.1095/biolreprod57.3.621
  56. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon-mediated signaling. Nat. Rev. Immunol. 5:375-386. https://doi.org/10.1038/nri1604
  57. Roberts, R. M., J. C. Cross and D. W. Leaman. 1992. Interferons as hormones of pregnancy. Endocrine Rev. 13:432-452.
  58. Robinson, S. J., H. Neal and W. R. Allen. 2000. Modulation of oviductal transport in mares by local application of prostaglandin E2. J. Reprod. Fertil. (Suppl 56):587-592.
  59. Rueda, B. R., K. A. Naivar, E. M. George, K. J. Austin, H. Francis and T. R. Hansen. 1993. Recombinant interferon-$\tau$ regulates secretion of two bovine endometrial proteins. J. Interferon Res. 13:295-301. https://doi.org/10.1089/jir.1993.13.295
  60. Satterfield, M. C., K. Hayashi, G. Song, S. G. Black, F. W. Bazer and T. E. Spencer. 2008. Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus. Biol. Reprod. 79:1226-1236. https://doi.org/10.1095/biolreprod.108.071787
  61. Schmitt, R. A., R. D. Geisert, M. T. Zavy, E. C. Short and R. M. Blair. 1993. Uterine cellular changes in 2',5'-oligoadenylate synthetase during the bovine estrous cycle and early pregnancy. Biol. Reprod. 48:460-466. https://doi.org/10.1095/biolreprod48.3.460
  62. Shamay, A., M. Pines, M. Waksman and A. Gertler. 1990. Proliferation of bovine mammary epithelial cells in vitro is modulated by G-proteins. Mol. Cell. Endocrinol. 69:217-226. https://doi.org/10.1016/0303-7207(90)90015-Z
  63. Short, E. C., R. D. Geisert, S. D. Helmer, M. T. Zavy and R. W. Fulton. 1991. Expression of antiviral activity and induction of 2',5' oligoadenylate synthetase by conceptus secretory proteins enriched in bovine trophoblast protein-1. Biol. Reprod. 44:261-268. https://doi.org/10.1095/biolreprod44.2.261
  64. Silvestre, F. T., T. S. M. Carvalho, N. Francisco, J. E. P. Santos, C. R. Staples, T. C. Jenkins and W. W. Thatcher. 2011. Effects of differential supplementation of fatty acids during the peripartum and breeding periods of Holstein cows: I. Uterine and metabolic responses, reproduction and lactation. J. Dairy Sci. 94:189-204. https://doi.org/10.3168/jds.2010-3370
  65. Silvia, W. J. and R. E. Raw. 1993. Activity of phospholipase C and release of prostaglandin $F_{2{\alpha}}$ by endometrial tissue from ewes during the oestrous cycle and early pregnancy. J. Reprod. Fertil. 97:529-537. https://doi.org/10.1530/jrf.0.0970529
  66. Simmons, R. M., M. C. Satterfield, T. H. Welsh, F. W. Bazer and T. E. Spencer. 2010. HSD11B1, HSD11B2, PTGS2 and NR3C1expression in the peri-implantation ovine uterus: effects of pregnancy,progesterone and interferon tau. Biol. Reprod. 82:35-43. https://doi.org/10.1095/biolreprod.109.079608
  67. Song, G., J. Y. Han, T. E. Spencer and F. W. Bazer. 2009. Interferon tau in the ovine uterus. J. Anim. Sci. Technol. 51:471-484. https://doi.org/10.5187/JAST.2009.51.6.471
  68. Spencer, T. E. and F. W. Bazer. 1995a. Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol. Reprod. 53:1527-1545. https://doi.org/10.1095/biolreprod53.6.1527
  69. Spencer, T. E., M. A. Mirando, T. F. Ogle and F. W. Bazer. 1995b. Ovine interferon-$\tau$ inhibits estrogen receptor up-regulation and estrogen-induced luteolysis in cyclic ewes. Endocrinology 136:4932-4944. https://doi.org/10.1210/en.136.11.4932
  70. Spencer, T. E., T. L. Ott, A. Gertler, E. Gootwine and F. W. Bazer. 1999. Effects of recombinant ovine interferon tau, placental lactogen and growth hormone on the ovine uterus. Biol. Reprod. 61:1409-1418. https://doi.org/10.1095/biolreprod61.6.1409
  71. Talamanates, F. and L.Ogren. 1988. The placenta as an endocrine organ. In: The Physiology of Reproduction: Polypeptides (Ed. E. Knobil and J. Neill), Raven Press Ltd, New York, pp. 2093-2144.
  72. Tamby, J. P., G. Charpigny, P. Reinaud and J. Martal. 1993. Phospholipase A2 activity in endometrium from early pregnant and non-pregnant ewes. Prostaglandins 46:407-415. https://doi.org/10.1016/0090-6980(93)90077-K
  73. Thatcher, W. W., M. D. Meyer and G. Danet-Desnoyers. 1995. Maternal recognition of pregnancy. J. Reprod. Fertil. (Suppl 49):15-28.
  74. Thatcher, W. W., C. R. Staples, G. Danet-Desnoyers, B. Oldick and E. P. Schmitt. 1994. Embryo health and mortality in sheep and cattle. J. Anim. Sci. 72(Suppl. 3):16-30.
  75. Vallet, J. L., P. J. Barker, G. E. Lamming, N. Skinner and N. S. Huskisson. 1991. A low molecular weight endometrial secretory protein which is increased by ovine trophoblast protein-1 is a beta 2-microglobulin-like protein. J. Endocrinol. 130:R1-R4. https://doi.org/10.1677/joe.0.130R001
  76. Weber, J. A., D. A. Freeman, D. K. Vanderwall and G. L. Woods. 1991. Prostaglandin E2 hastens oviductal transport of equine embryos. Biol. Reprod. 45:544-546. https://doi.org/10.1095/biolreprod45.4.544
  77. Xavier, F., M. Guillomot, M. Charlier, J. Martal and P. Gaye. 1991. Co-expression of the protooncogene FOS (cfos) and an embryonic interferon (ovine trophoblastin) by sheep conceptuses during implantation. Biol. Cell 73:27-33. https://doi.org/10.1016/0248-4900(91)90005-8
  78. Yankey, S. J., B. A. Hicks, K. G. Carnahan, A. M. Assiri, S. J. Sinor, K. Kodali, J. N. Stellflug and T. L. Ott. 2001. Expression of the antiviral protein Mx in peripheral blood mononuclear cells of pregnant and bred, non-pregnant ewes. J. Endocrinol. 170:R7-R11. https://doi.org/10.1677/joe.0.170R007
  79. Young, K. H., R. R. Kraeling and F. W. Bazer. 1989. Effects of prolactin on conceptus survival land uterine secretory activity in pigs. J. Reprod. Fertil. 86:713-722. https://doi.org/10.1530/jrf.0.0860713
  80. Yu-Lee, L. Y., J. A. Hrachovy, A. M. Stevens and L. A. Schwarz. 1990. Interferon regulatory factor 1 is an immediate-early gene under transcriptional regulation by prolactin in Nb2 T cells. Mol. Cell. Biol. 10:3087-3094.

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