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Effects of 17β-estradiol, Interleukin-1β, and Human Chorionic Gonadotropin on Activity and mRNA Expression of Plasminogen Activators in Porcine Endometrial Cells

  • Hwangbo, Yong (College of Animal Life Sciences, Kangwon National University) ;
  • Cheong, Hee-Tae (College of Veterinary Medicine, Kangwon National University) ;
  • Yang, Boo-Keun (College of Animal Life Sciences, Kangwon National University) ;
  • Park, Choon-Keun (College of Animal Life Sciences, Kangwon National University)
  • 투고 : 2018.06.06
  • 심사 : 2018.06.26
  • 발행 : 2018.06.30

초록

This study aimed to investigate changes in the activity and mRNA expression of plasminogen activators (PAs) induced by $17{\beta}$-estradiol ($E_2$), human chorionic gonadotropin (hCG), and interleukin-$1{\beta}$ ($IL-1{\beta}$) in porcine endometrial cells. Endometrial cells were isolated from the epithelium and cultured to 80% confluence. They were then treated for 24 h with $E_2$ (0.2, 2, 20, and 200 ng/mL), $IL-1{\beta}$ (0.1, 1, 10, and 100 ng/mL), and hCG (0.5, 1, 1.5 and 2 IU/mL). mRNA expressions of urokinase-type (uPA) and tissue-type (tPA) PAs were analyzed using reverse transcription PCR, and activities were measured using a PA activity assay. mRNA expressions of uPA and tPA increased with $E_2$ treatment; however, this was not significant. Similarly, treatment with hCG did not influence the mRNA expressions of PAs. Interestingly, treatment with 0.1 ng/mL $IL-1{\beta}$ significantly reduced the mRNA expression of uPA, but did not affect that of tPA. Treatment with 2, 20, and 200 ng/mL $E_2$ increased PA activity compared with the control group; treatment with 0.1 and 1 ng/mL $IL-1{\beta}$ significantly increased PA activity compared with the other $IL-1{\beta}$ treatment groups, whereas treatment with 10 and 100 ng/mL $IL-1{\beta}$ decreased. Treatment with 2 IU/mL hCG increased PA activity compared with the other treatment groups, although there were no significant differences between the hCG and control groups. In conclusion, the activity and mRNA expression of PAs were differently regulated by the hormone/cytokine and its concentration in porcine endometrial cells. Therefore, understanding PA regulatory mechanisms may help to improve the reproductive potential of domestic animals.

키워드

참고문헌

  1. Ahn SH, Cheong HT, Yang BK, Kim DY, Park CK (2009) Relationship between plasminogen activity and plasminogen inhibitor during the culture of porcine oviduct epithelial cells. Reprod Dev Biol 33:203-209.
  2. Baker VL, Draper M, Paul S, Allerheiligen S, Glant M, Shifren J, Jaffe RB (1998) Reproductive endocrine and endometrial effects of raloxifene hydrochloride, a selective estrogen receptor modulator, in women with regular menstrual cycles 1. J Clin Endocrinol Metab 83:6-13.
  3. Bazer FW, Johnson GA (2014) Pig blastocyst-uterine interactions. Differentiation 87:52-65. https://doi.org/10.1016/j.diff.2013.11.005
  4. Beers WH (1975) Follicular plasminogen and plasminogen activator and the effect of plasmin on ovarian follicle wall. Cell 6:379-386. https://doi.org/10.1016/0092-8674(75)90187-7
  5. Bolzan E, Andronowska A, Bodek G, Morawska-Pucinska E, Krawczynski K, Dabrowski A, Ziecik AJ (2013) The novel effect of hCG administration on luteal function maintenance during the estrous cycle/pregnancy and early embryo development in the pig. Pol J Vet Sci 16:323-332. https://doi.org/10.2478/pjvs-2013-0044
  6. Brussow KP, Schneider F, Kanitz W, Ratky J, Kauffold J, Wahner M (2009) Studies on fixed-time ovulation induction in the pig. Soc Reprod Fertil Suppl 66:187-195.
  7. Cheon YP (2007) Altering of collagens in early pregnant mouse uterus. Dev Reprod 11:1-11.
  8. Cheon YP, Lee DM, Chun TH, Lee KH, Choi IH (2009) Androgen in the uterus: A compensator of estrogen and progesterone. Dev Reprod 13:133-143.
  9. Coy P, Jimenez-Movilla M, Garcia-Vazquez FA, Mondejar I, Grullon L, Romar R (2012) Oocytes use the plasminogen-plasmin system to remove supernumerary spermatozoa. Hum Reprod 27:1985-1993. https://doi.org/10.1093/humrep/des146
  10. Demir R, Yaba A, Huppertz B (2010) Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation. Acta Histochem 112:203-214. https://doi.org/10.1016/j.acthis.2009.04.004
  11. Ebisch IMW, Thomas CMG, Wetzels AMM, Willemsen WNP, Sweep FCGJ, Steegers-Theunissen RPM (2008) Review of the role of the plasminogen activators system and vascular endothelial growth factor in subfertility. Fertil Steril 90:2340-2350. https://doi.org/10.1016/j.fertnstert.2007.10.026
  12. Finlay TH, Katz J, Kirsch L, Levitz M, Nathoo SA, Seiler S (1983) Estrogen-stimulated uptake of plasminogen by the mouse uterus. Endocrinology 112:856-861. https://doi.org/10.1210/endo-112-3-856
  13. Franczak A, Wojciechowicz B, Kotwica G (2013) Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle. Reprod Biol 13:229-237. https://doi.org/10.1016/j.repbio.2013.07.001
  14. Giordano JO, Wiltbank MC, Guenther JN, Ares MS, Lopes Jr G, Herlihy MM, Fricke PM (2012) Effect of presynchronization with human chorionic gonadotropin or gonadotropin-releasing hormone 7 days before resynchronization of ovulation on fertility in lactating dairy cows. J Dairy Sci 95:5612-5625. https://doi.org/10.3168/jds.2011-5035
  15. Hwangbo Y, Lee SH, Cha HJ, Song EJ, Lee ST, Lee ES, Cheong HT, Yang BK, Park CK (2013) Expression of plasminogen activators in uterine epithelial cells of pre-ovulatory phase in pigs. J Emb Trans 28:257-263. https://doi.org/10.12750/JET.2013.28.3.257
  16. Jeong W, Kim J, Bazer FW, Song G, Kim J (2016) Stimulatory effects of interleukin-1 beta on development of porcine uterine epithelial cell are mediated by activation of the ERK1/2 MAPK cell signaling cascade. Mol Cell Endocrinol 419:225-234. https://doi.org/10.1016/j.mce.2015.10.022
  17. Kim KH, Lee YS, Gu HN, Yang BK, Cheong HT, Park CK (2011) Changes in plasminogen activity in uterus tissue during the estrous cycle in the pigs. Reprod Dev Biol 35:463-468.
  18. Kobayashi T, Matsuda Y, Park JY, Hara I, Kaneko S, Fujimoto Y, Nozawa S, Akihama S (1992) Trypsin-like arginine amidases including plasminogen and plasmin in human seminal plasma by affinity adsorption and elution. Arch Androl 28:165-170. https://doi.org/10.3109/01485019208987694
  19. Kouba AJ, Burkhardt BR, Alvarez IM, Goodenow MM, Buhi WC (2000) Oviductal plasminogen activator inhibitor (PAI-1): mRNA, protein, and hormonal regulation during the estrous cycle and early pregnancy in the pig. Mol Reprod Dev 56:378-386. https://doi.org/10.1002/1098-2795(200007)56:3<378::AID-MRD8>3.0.CO;2-B
  20. Krania F, Dovolou E, Rekkas CA, Theodosiadou EK, Pappas I, Amiridis GS (2015) Effects of addition of tissuetype plasminogen activator in in vitro fertilization medium on bovine embryo development and quality. Reprod Domest Anim 50:112-120. https://doi.org/10.1111/rda.12456
  21. Lai MD, Lee LR, Cheng KS, Wing LY (2000) Expression of proliferating cell nuclear antigen in luminal epithelium during the growth and regression of rat uterus. J Endocrinol 166:87-93. https://doi.org/10.1677/joe.0.1660087
  22. Liu YX, Cajander SB, Ny T, Kristensen P, Hsueh AJW (1987) Gonadotropin regulation of tissue-type and urokinase-type plasminogen activators in rat granulosa and theca-interstitial cells during the periovulatory period. Mol Cell Endocrinol 54:221-229. https://doi.org/10.1016/0303-7207(87)90160-2
  23. Malysz-Cymborska I, Ziecik AJ, Waclawik A, Andronowska A (2013) Effect of hCG and eCG treatments on prostaglandins synthesis in the porcine oviduct. Reprod Domest Anim 48:1034-1042. https://doi.org/10.1111/rda.12210
  24. Martin O, Arias F (1982) Plasminogen activator production by trophoblast cells in vitro: Effect of steroid hormones and protein synthesis inhibitors. Am J Obstet Gynecol 142:402-409. https://doi.org/10.1016/S0002-9378(16)32380-8
  25. Menshikov M, Plekhanova O, Cai H, Chalupsky K, Parfyonova Y, Bashtrikov P, Tkachuk V, Berk BC (2006) Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol 26:801-807. https://doi.org/10.1161/01.ATV.0000207277.27432.15
  26. Ny T, Bjersing L, Hsueh AJW, Loskutoff DJ (1985) Cultured granulosa cells produce two plasminogen activators and an ant iactivator, each regulated differently by gonadotropins. Endocrinology 166:1666-1668.
  27. Olofsson B, Korpelainen E, Pepper MS, Mandriota SJ, Aase K, Kumar V, Gunji Y, Jeltsch MM, Shibuya M, Alitalo K, Eriksson U (1998) Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 95:11709-11714. https://doi.org/10.1073/pnas.95.20.11709
  28. Ploplis VA, French EL, Carmeliet P, Collen D, Plow EF (1998) Plasminogen deficiency differentially affects recruitment of inflammatory cell populations in mice. Blood 91:2005-2009.
  29. Ross JW, Ashworth MD, Hurst AG, Malayer JR, Geisert RD (2003) Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reprod Biol Endocrinol 1:23. https://doi.org/10.1186/1477-7827-1-23
  30. Sa SJ, Park CK, Kim IC, Lee SH, Kwon OS, Kim MJ, Cho KH, Kim DW, So KM, Cheong HT (2010) Effects of reactive oxygen species (ROS) on sperm function and plasminogen activator activity in porcine spermatozoa. Reprod Dev Biol 34:185-191.
  31. Shemesh M, Mizrachi D, Gurevich M, Shore LS, Reed J, Chang SM, Thatcher WW, Fields MJ (2001) Expression of functional luteinizing hormone (LH) receptor and its messenger ribonucleic acid in bovine endometrium: LH augmentation of cAMP and inositol phosphate in vitro and human chorionic gonadotropin (hCG) augmentation of peripheral prostaglandin in vivo. Reprod Biol 1:13-32.
  32. Stormshak F, Bishop CV (2008) Board-invited review: Estrogen and progesterone signaling: Genomic and nongenomic actions in domestic ruminants. J Anim Sci 86:299-315. https://doi.org/10.2527/jas.2007-0489
  33. Stroband HWJ, Taverne N, Langenfeld K, Barends PMG (1986) The ultrastructure of the uterine epithelium of the pig during the estrous cycle and early pregnancy. Cell Tissue Res 246:81-89.
  34. Subramaniam S, Stansberg C, Cunningham C (2004) The interleukin 1 receptor family. Dev Comp Immunol 28:415-428. https://doi.org/10.1016/j.dci.2003.09.016
  35. Sugino N (2014) Molecular mechanisms of luteinization. Obstet Gynecol Sci 57:93-101. https://doi.org/10.5468/ogs.2014.57.2.93
  36. Wongkaweewit K, Prommachart P, Raksasub R, Buranaamnuay K, Techakumphu M, De Rensis F, Tummaruk P (2012) Effect of the administration of GnRH or hCG on time of ovulation and the onset of estrus-toovulation interval in sows in Thailand. Trop Anim Health Pro 44:467-470. https://doi.org/10.1007/s11250-011-9920-3