Changes in Plasminogen Activity in Uterus Tissue during the Estrous Cycle in the Pigs

  • Kim, Kang-Hyun (College of Animal Life Sciences, Kangwon National University) ;
  • Lee, Yong-Seung (College of Animal Life Sciences, Kangwon National University) ;
  • Gu, Ha-Na (College of Animal Life Sciences, Kangwon National University) ;
  • Yang, Boo-Keun (College of Animal Life Sciences, Kangwon National University) ;
  • Cheong, Hee-Tae (College of Veterinary Medicine, Kangwon National University) ;
  • Park, Choon-Keun (College of Animal Life Sciences, Kangwon National University)
  • Received : 2011.11.11
  • Accepted : 2011.11.21
  • Published : 2011.12.31

Abstract

This study investigated the changes of plasminogen activators (PAs) activity, expression and localization of tissue plasminogen activator (tPA) and urokinase plasminogen activator (uPA) during the estrous cycle in pigs. Estrous cycle was sorted into three group by pre-ovulation (Pre-Ov), post-ovulation (Post-Ov) and early to mid-luteal stages (Early to mid-L). Analysis for immunohistochemistry was confirmed by location of tPA and uPA. Porcine uterus tissue was cut into $1{\times}1$ cm squares, and were incubated in DMEM/F-12 medium for 1 h at $38^{\circ}C$, 5% $CO_2$ for measurement of PA activity. Western blotting was implemented for measurement of PA quantity. In results, the blood vessels and secretory glands were increased in Post-Ov stage than Pre-Ov and Early to mid-L stages. The tPA and uPA was located mainly within lumen of blood vessels and secretory glands. The PA activity in Post-Ov ($0.99{\pm}0.03$) stage were significantly (p<0.01) higher than Pre-Ov stage ($0.51{\pm}0.03$) and Early to mid-L stage ($0.21{\pm}0.04$). Expression of PAs were significantly (p<0.05) higher in Early to mid-L stage than other stages. These results indicate that PAs activity and expression may change in uterus tissue during the estrous cycle in pigs.

Keywords

References

  1. Beers WH (1975): Follicular plasminogen and plasminogen activator and effects of plasmin on ovarian follicle wall. Cell 6:379-386. https://doi.org/10.1016/0092-8674(75)90187-7
  2. Casslen B, Astedt B (1983): Occurrence of both urokinase and tissue plasminogen activator in the human endometrium. Contraception 28(6):553-564. https://doi.org/10.1016/0010-7824(83)90106-3
  3. Casslen B, Nordengren J, Gustavsson B, Nilbert M, Lund LR (1995): Progesterone stimulates degradation of urokinase plasminogen activator (u-PA) in endometrial stromal cells by increasing its inhibitor (PAI1) and surface expression of the u-PA receptor. J Clin Endocrinol Metab 80:2776-2784. https://doi.org/10.1210/jc.80.9.2776
  4. Chern SR, Li SH, Lu CH, Chen EIT (2010): Spatiotemporal expression of the serine protease inhibitor, SERPINE2, in the mouse placenta and uterus during the estrous cycle, pregnancy, and lactation. RB & E 8:127.
  5. Dano K, Andersen PA, Grondahl-Hansen J, Kristensen P, Nilsen LS, Skriver J (1985): Plasminogen activators, tissue degradation and cancer. Adv Cancer Res 44:139-266.
  6. Dudek GA, Kloczewiak M, Budzynski AZ, Latallo ZS, Kopec M (1970): Characterisation and comparison of macromolecular and products of fibrinogen and fibrin proteolysis by plasmin. Biochim Biophys Acta 214:44-51. https://doi.org/10.1016/0005-2795(70)90068-1
  7. Enisch IM, Thomas CM, Wetzels AM, Willemsen WN, Sweep FC, Steegers-Theunissen RP (2008): Review of the role of the plasminogen activator system and vascular endothelial growth factor in subfertility. Fertil Steril 90(6):2340-2350. https://doi.org/10.1016/j.fertnstert.2007.10.026
  8. 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
  9. Floridon C, Nielsen O, Holund B, Sunde L, Westergaard JG, Thomasen SG, Teisner B (1999): Localization and significance of urokinase plasminogen activator and its receptor in placental tissue from intrauterin, Ectopic and molar pregnancies. Placenta 20:711-721. https://doi.org/10.1053/plac.1999.0425
  10. Gabler C, Killian GJ, Einspanier R (2001): Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle. Reproduction 122:121-130. https://doi.org/10.1530/rep.0.1220121
  11. Ghosh D, Sengupta J (1998). Recent developments in endocrinology and paracrinology of blastocyst implantation in the primate. Hum Reprod Update 4: 153-168. https://doi.org/10.1093/humupd/4.2.153
  12. Hart DA, Rehemtulla A (1988): Plasminogen activators and their inhibitors: regulators of extracellular proteolysis and cell function. Comparative biochemistry and physiology B. Comparative Biochemistry 90:691-708.
  13. Huarte J, Belin D, Vassalli JD (1985): Plasminogen activator in mouse and rat oocytes: induction during meiotic maturation. Cell 43:551-558. https://doi.org/10.1016/0092-8674(85)90184-9
  14. Irigoyen JP, Munoz-Canoves P, Montero L, Koziczak M, Nagamine Y (1999): The plasminogen activator system: biology and regulation. Cell Mol Life Sci 55:104-132.
  15. Jimenez Diaz M, Giunta S, Valz-Gianinet J, Pereyra- Alfonso S, Flores V, Miceli D (2000): Proteases with plasminogen activator activity in hamster oviduct. Mol Reprod Dev 55:47-45. https://doi.org/10.1002/(SICI)1098-2795(200001)55:1<47::AID-MRD7>3.0.CO;2-J
  16. Liotta LA, Goldfarb RH, Brundage R, Siegal GP, Terranova V, Garbisa S (1981): Effect of plasminogen activator (urokinase), plasmin and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res 41:4629-4636.
  17. 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
  18. Mignatti P, Rifkin DB (1993): Biology and biochemistry of proteinase in tumor invasion. Physiol Rev 73:161-195. https://doi.org/10.1152/physrev.1993.73.1.161
  19. Miles LA, Plow EF (1987): Receptor mediated binding of the fibrinolytic components, plasminogen and urokinase, to peripheral blood cells. JTH 58(3):936- 942.
  20. O 'Connell ML, Caniparis R, Strickland S (1987): Hormonal regulation of tissue plasminogen activator secretion and mRNA levels in rat granulosa cells. J Biol Chemistry 262(5): 2339-2344.
  21. Rajput B, Degen SF, Reich E, Waller EK, Axelord J, Eddy RL (1985): Chromosomal locations of human tissue plasminogen activator and urokinase genes. Science 230:672-674. https://doi.org/10.1126/science.3840278
  22. Roldan-Olarte M, Jimenez-Diaz M, Miceli DC (2005): Plasminogen detection in oocytes and plasminogen activator activities in the porcine oviduct during the estrous cycle. Zygote 13. Cambridge, UK, pp 115- 123.
  23. Sandberg T, Casslen B, Gustavsson B, Benraad TJ (1998): Human endothelial cell migration is stimulated by urokinase plasminogen activator: plasminogen activator inhibitor 1 complex released from endometrial stromal cells stimulated with transforming growth factor b1; possible mechanism for paracrine stimulation of endometrial angiogenesis. Biol Reprod 59:759-767. https://doi.org/10.1095/biolreprod59.4.759
  24. Saksela O, Rifkin DB (1988): Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol 4:93-126. https://doi.org/10.1146/annurev.cb.04.110188.000521
  25. Sappino AP, Huarte J, Belin D, Vassalli JD (1989): Plasminogen activators in tissue remodelling and invasion: mRNA localisation in mouse ovaries and implanting embryos. J Cell Biol 109:2471-2479. https://doi.org/10.1083/jcb.109.5.2471
  26. Smokovitis A, Kokolis N, Alexopoulos C, Alexaki E, Eleftheriou E (1987): Plasminogen activator activity, plasminogen activator inhibition and plasmin inhibition in spermatozoa and seminal plasma of man and various animal species: Effect of plasmin on sperm motility. Fibrinolysis 1:253-257. https://doi.org/10.1016/0268-9499(87)90045-2
  27. Strickland S, Reich E, Sherman MI (1976): Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm. Cell Oct 9(2):231-240. https://doi.org/10.1016/0092-8674(76)90114-8
  28. Teesalu T, Blasi F, Talarico D (1996): Embryo implantation in mouse: fetomaternal coordination in the pattern of expression of uPA, uPAR, PAI-1 and $\alpha$ 2MR/LRP genes. Mech Dev 56:103-116. https://doi.org/10.1016/0925-4773(96)00515-1
  29. Tonner E, Allan GJ, Flint DJ (2000): Hormonal control of plasmin and tissue-type plasminogen activator activity in rat milk during involution of the mammary gland. J Endocrinology 167:265-273. https://doi.org/10.1677/joe.0.1670265
  30. Vassalli JD, Sappino AP, Belin D (1991): The plasminogen activator/plasmin system. J Clin Invest 88: 1067-1072. https://doi.org/10.1172/JCI115405
  31. Zaneveld JL, Polakoski KL, Schumacher GF (1975): Proteases and Biological Control. New York: Cold Spring Harbor pp 683-706.