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BioMed Research International
Volume 2015, Article ID 808146, 11 pages
http://dx.doi.org/10.1155/2015/808146
Clinical Study

Abnormal Expression of Prostaglandins E2 and F2α Receptors and Transporters in Patients with Endometriosis

1Centre Hospitalier Universitaire de Québec, Québec, Canada G1V 4G2
2Faculté de Médecine, Université Laval, Québec, Canada G1V 0A6

Received 16 September 2014; Revised 25 November 2014; Accepted 8 December 2014

Academic Editor: Andrea Tinelli

Copyright © 2015 Halima Rakhila et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. C. Giudice, “Clinical practice. Endometriosis,” The New England Journal of Medicine, vol. 362, no. 25, pp. 2389–2398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Akoum, A. Lemay, C. Brunet, and J. Hebert, “Secretion of monocyte chemotactic protein-1 by cytokine-stimulated endometrial cells of women with endometriosis,” Fertility and Sterility, vol. 63, no. 2, pp. 322–328, 1995. View at Google Scholar · View at Scopus
  3. Y. Yang, P. Degranpré, A. Kharfi, and A. Akoum, “Identification of macrophage migration inhibitory factor as a potent endothelial cell growth-promoting agent released by ectopic human endometrial cells,” The Journal of Clinical Endocrinology & Metabolism, vol. 85, no. 12, pp. 4721–4727, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Khoufache, P. K. Bondza, N. Harir et al., “Soluble human IL-1 receptor type 2 inhibits ectopic endometrial tissue implantation and growth: identification of a novel potential target for endometriosis treatment,” The American Journal of Pathology, vol. 181, no. 4, pp. 1197–1205, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Y. Dawood, F. S. Khan-Dawood, and L. Wilson Jr., “Peritoneal fluid prostaglandins and prostanoids in women with endometriosis, chronic pelvic inflammatory disease, and pelvic pain,” American Journal of Obstetrics & Gynecology, vol. 148, no. 4, pp. 391–395, 1984. View at Publisher · View at Google Scholar · View at Scopus
  6. T.-C. Lee and H.-C. Ho, “Effects of prostaglandin E2 and vascular endothelial growth factor on sperm might lead to endometriosis-associated infertility,” Fertility and Sterility, vol. 95, no. 1, pp. 360–362, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. A. I. Koskimies, A. Tenhunen, and O. Ylikorkala, “Peritoneal fluid 6-ketoprostaglandin F1α, thromboxane B2 in endometriosis and unexplained infertility,” Acta Obstetricia et Gynecologica Scandinavica, vol. 63, no. 123, pp. 19–21, 1984. View at Publisher · View at Google Scholar · View at Scopus
  8. S. H. Ferreira, “Prostaglandins, pain, and inflammation,” Agents and Actions Supplements, vol. 19, pp. 91–98, 1986. View at Google Scholar · View at Scopus
  9. M. S. Arayne and S. S. Ul Hasan, “Prostaglandins: in pain and inflammatiin,” Journal of the Pakistan Medical Association, vol. 27, no. 5, pp. 326–330, 1977. View at Google Scholar · View at Scopus
  10. O. Ylikorkala, A. Koskimies, T. Laatkainen, A. Tenhunen, and L. Viinikka, “Peritoneal fluid prostaglandins in endometriosis, tubal disorders, and unexplained infertility,” Obstetrics and Gynecology, vol. 63, no. 5, pp. 616–620, 1984. View at Google Scholar · View at Scopus
  11. N. M. Pobedinskiǐ, M. A. Khachikian, V. P. Zykova, and N. D. Fanchenko, “Blood levels of prostaglandins in fertile women and in women with different variants of endocrine infertility,” Akusherstvo i Ginekologiia, no. 8, pp. 14–18, 1982. View at Google Scholar · View at Scopus
  12. R. S. Schenken, R. H. Asch, R. F. Williams, and G. D. Hodgen, “Etiology of infertility in monkeys with endometriosis: measurement of peritoneal fluid prostaglandins,” American Journal of Obstetrics and Gynecology, vol. 150, no. 4, pp. 349–353, 1984. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Shirasuna, K. Sasahara, M. Matsui, T. Shimizu, and A. Miyamoto, “Prostaglandin F2α differentially affects mRNA expression relating to angiogenesis, vasoactivation and prostaglandins in the early and mid corpus luteum in the cow,” Journal of Reproduction and Development, vol. 56, no. 4, pp. 428–436, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Majima, H. Amano, and I. Hayashi, “Endogenous prostaglandins and angiogenesis,” Nihon Yakurigaku Zasshi, vol. 117, no. 4, pp. 283–292, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Ulug, S. Goldman, I. Ben-Shlomo, and E. Shalev, “Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F2α and indomethacin,” Molecular Human Reproduction, vol. 7, no. 12, pp. 1187–1193, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. H.-H. Hsu, W.-S. Hu, Y.-M. Lin et al., “JNK suppression is essential for 17β-Estradiol inhibits prostaglandin E2-Induced uPA and MMP-9 expressions and cell migration in human LoVo colon cancer cells,” Journal of Biomedical Science, vol. 18, no. 1, article 61, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Ota, S. Igarashi, M. Sasaki, and T. Tanaka, “Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis,” Human Reproduction, vol. 16, no. 3, pp. 561–566, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Carli, C. N. Metz, Y. Al-Abed, P. H. Naccache, and A. Akoum, “Up-regulation of cyclooxygenase-2 expression and prostaglandin E2 production in human endometriotic cells by macrophage migration inhibitory factor: involvement of novel kinase signaling pathways,” Endocrinology, vol. 150, no. 7, pp. 3128–3137, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Fan and X. L. Fang, “Expression of cylooxygenase-2 in endometriosis,” Zhong Nan Da Xue Xue Bao Yi Xue Ban, vol. 30, no. 1, pp. 92–95, 2005. View at Google Scholar
  20. S. K. Banu, J. Lee, V. O. Speights Jr., A. Starzinski-Powitz, and J. A. Arosh, “Cyclooxygenase-2 regulates survival, migration, and invasion of human endometriotic cells through multiple mechanisms,” Endocrinology, vol. 149, no. 3, pp. 1180–1189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. E. A. Willman, W. P. Collins, and S. G. Clayton, “Studies in the involvement of prostaglandins in uterine symptomatology and pathology,” BJOG, vol. 83, no. 5, pp. 337–341, 1976. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Lundstrom, K. Green, and K. Svanborg, “Endogenous prostaglandins in dysmenorrhea and the effect of prostaglandin synthetase inhibitors (PGSI) on uterine contractility,” Acta Obstetricia et Gynecologica Scandinavica, vol. 58, no. 87, pp. 51–56, 1979. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Stromberg, M. Akerlund, M. L. Forsling, and H. Kindahl, “Involvement of prostaglandins in vasopressin stimulation of the human uterus,” British Journal of Obstetrics & Gynaecology, vol. 90, no. 4, pp. 332–337, 1983. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Z. A. Badawy, V. Cuenca, and L. Marshall, “Peritoneal fluid prostaglandins in patients with endometriosis,” Contributions to Gynecology and Obstetrics, vol. 16, pp. 60–65, 1987. View at Google Scholar · View at Scopus
  25. S. Z. A. Badawy, L. Marshall, and V. Cuenca, “Peritoneal fluid prostaglandins in various stages of the menstrual cycle: role in infertile patients with endometriosis,” International Journal of Fertility, vol. 30, no. 2, pp. 48–52, 1985. View at Google Scholar · View at Scopus
  26. H. Rakhila, C. Carli, M. Daris, M. Lemyre, M. Leboeuf, and A. Akoum, “Identification of multiple and distinct defects in prostaglandin biosynthetic pathways in eutopic and ectopic endometrium of women with endometriosis,” Fertility and Sterility, vol. 100, no. 6, pp. 1650.e2–1659.e2, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. H. N. Jabbour and K. J. Sales, “Prostaglandin receptor signalling and function in human endometrial pathology,” Trends in Endocrinology and Metabolism, vol. 15, no. 8, pp. 398–404, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. H. N. Jabbour, K. J. Sales, O. P. M. Smith, S. Battersby, and S. C. Boddy, “Prostaglandin receptors are mediators of vascular function in endometrial pathologies,” Molecular and Cellular Endocrinology, vol. 252, no. 1-2, pp. 191–200, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Lee, J. A. McCracken, S. K. Banu, and J. A. Arosh, “Intrauterine inhibition of prostaglandin transporter protein blocks release of luteolytic PGF2alpha pulses without suppressing endometrial expression of estradiol or oxytocin receptor in ruminants,” Biology of Reproduction, vol. 89, no. 2, article 27, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Chi and V. L. Schuster, “The prostaglandin transporter PGT transports PGH2,” Biochemical and Biophysical Research Communications, vol. 395, no. 2, pp. 168–172, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Lacroix-Pépin, G. Danyod, N. Krishnaswamy et al., “The multidrug resistance-associated protein 4 (MRP4) appears as a functional carrier of prostaglandins regulated by oxytocin in the bovine endometrium,” Endocrinology, vol. 152, no. 12, pp. 4993–5004, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. M.-H. Wu, Y. Shoji, P.-C. Chuang, and S.-J. Tsai, “Endometriosis: disease pathophysiology and the role of prostaglandins,” Expert Reviews in Molecular Medicine, vol. 9, no. 2, pp. 1–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. M. A. Lumsden, R. W. Kelly, M. H. Abel, and D. T. Baird, “The concentrations of prostaglandins in endometrium during the menstrual cycle in women with measured menstrual blood loss,” Prostaglandins Leukotrienes and Medicine, vol. 23, no. 2-3, pp. 217–227, 1986. View at Publisher · View at Google Scholar · View at Scopus
  34. S. A. Milne, G. B. Perchick, S. C. Boddy, and H. N. Jabbour, “Expression, localization, and signaling of PGE2 and EP2/EP4 receptors in human nonpregnant endometrium across the menstrual cycle,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 9, pp. 4453–4459, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. P. Rees, A. B. M. Anderson, L. M. Demers, and A. C. Turnbull, “Endometrial and myometrial prostaglandin release during the menstrual cycle in relation to menstrual blood loss,” The Journal of Clinical Endocrinology & Metabolism, vol. 58, no. 5, pp. 813–818, 1984. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Kang, P. Chapdelaine, J. Parent, E. Madore, P. Y. Laberge, and M. A. Fortier, “Expression of human prostaglandin transporter in the human endometrium across the menstrual cycle,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 4, pp. 2308–2313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Namba, Y. Sugimoto, M. Negishi et al., “Alternative splicing of C-terminal tail of prostaglandin E receptor subtype EP3 determines G-protein specificity,” Nature, vol. 365, no. 6442, pp. 166–170, 1993. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Sakamoto, T. Ezashi, K. Miwa et al., “Molecular cloning and expression of a cDNA of the bovine prostaglandin F2α receptor,” The Journal of Biological Chemistry, vol. 269, no. 5, pp. 3881–3886, 1994. View at Google Scholar · View at Scopus
  39. J. A. Arosh, S. K. Banu, P. Chapdelaine et al., “Molecular cloning and characterization of bovine prostaglandin E2 receptors EP2 and EP4: expression and regulation in endometrium and myometrium during the estrous cycle and early pregnancy,” Endocrinology, vol. 144, no. 7, pp. 3076–3091, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Narumiya, Y. Sugimoto, and F. Ushikubi, “Prostanoid receptors: structures, properties, and functions,” Physiological Reviews, vol. 79, no. 4, pp. 1193–1226, 1999. View at Google Scholar · View at Scopus
  41. S. Narumiya and G. A. FitzGerald, “Genetic and pharmacological analysis of prostanoid receptor function,” The Journal of Clinical Investigation, vol. 108, no. 1, pp. 25–30, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Ueno, H. Matsumoto, H. Naraba et al., “Major roles of prostanoid receptors IP and EP3 in endotoxin-induced enhancement of pain perception,” Biochemical Pharmacology, vol. 62, no. 2, pp. 157–160, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Minami, H. Nakano, T. Kobayashi et al., “Characterization of EP receptor subtypes responsible for prostaglandin E2-induced pain responses by use of EP1 and EP3 receptor knockout mice,” British Journal of Pharmacology, vol. 133, no. 3, pp. 438–444, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. J. A. Richards and R. W. Brueggemeier, “Prostaglandin E2 regulates aromatase activity and expression in human adipose stromal cells via two distinct receptor subtypes,” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 6, pp. 2810–2816, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Sennlaub, F. Valamanesh, A. Vazquez-Tello et al., “Cyclooxygenase-2 in human and experimental ischemic proliferative retinopathy,” Circulation, vol. 108, no. 2, pp. 198–204, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. P.-C. Chuang, H. S. Sun, T.-M. Chen, and S.-J. Tsai, “Prostaglandin E2 induces fibroblast growth factor 9 via EPS-dependent protein kinase Cδ and Elk-1 signaling,” Molecular and Cellular Biology, vol. 26, no. 22, pp. 8281–8292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. K. J. Sales, S. A. Milne, A. R. W. Williams, R. A. Anderson, and H. N. Jabbour, “Expression, localization, and signaling of prostaglandin F2α receptor in human endometrial adenocarcinoma: regulation of proliferation by activation of the epidermal growth factor receptor and mitogen-activated protein kinase signaling pathways,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 2, pp. 986–993, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Lee, S. K. Banu, R. C. Burghardt, A. Starzinski-Powitz, and J. A. Arosh, “Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits adhesion of human endometriotic epithelial and stromal cells through suppression of integrin-mediated mechanisms,” Biology of Reproduction, vol. 88, no. 3, p. 77, 2013. View at Publisher · View at Google Scholar
  49. J. Lee, S. K. Banu, R. Rodriguez, A. Starzinski-Powitz, and J. A. Arosh, “Selective blockade of prostaglandin E2 receptors EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest,” Fertility and Sterility, vol. 93, no. 8, pp. 2498–2506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Lee, S. K. Banu, T. Subbarao, A. Starzinski-Powitz, and J. A. Arosh, “Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits invasion of human immortalized endometriotic epithelial and stromal cells through suppression of metalloproteinases,” Molecular and Cellular Endocrinology, vol. 332, no. 1-2, pp. 306–313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. K. L. Pierce, H. Fujino, D. Srinivasan, and J. W. Regan, “Activation of FP prostanoid receptor isoforms leads to rho-mediated changes in cell morphology and in the cell cytoskeleton,” Journal of Biological Chemistry, vol. 274, no. 50, pp. 35944–35949, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Sheng, J. Shao, M. K. Washington, and R. N. DuBois, “Prostaglandin E2 increases growth and motility of colorectal carcinoma cells,” Journal of Biological Chemistry, vol. 276, no. 21, pp. 18075–18081, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. V. Capra, A. Habib, M. R. Accomazzo et al., “Thromboxane prostanoid receptor in human airway smooth muscle cells: a relevant role in proliferation,” European Journal of Pharmacology, vol. 474, no. 2-3, pp. 149–159, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. I. Gori, Y. Rodriguez, C. Pellegrini et al., “Augmented epithelial multidrug resistance-associated protein 4 expression in peritoneal endometriosis: regulation by lipoxin A4,” Fertility and Sterility, vol. 99, no. 7, pp. 1965.e2–1973.e2, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. L. H. Lye, J. G. Kench, D. J. Handelsman et al., “Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer,” The Prostate, vol. 68, no. 13, pp. 1421–1429, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Copsel, C. Garcia, F. Diez et al., “Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation,” The Journal of Biological Chemistry, vol. 286, no. 9, pp. 6979–6988, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. V. R. Holla, M. G. Backlund, P. Yang, R. A. Newman, and R. N. DuBois, “Regulation of prostaglandin transporters in colorectal neoplasia,” Cancer Prevention Research, vol. 1, no. 2, pp. 93–99, 2008. View at Publisher · View at Google Scholar
  58. K. Guda, S. P. Fink, G. L. Milne et al., “Inactivating mutation in the prostaglandin transporter gene, SLCO2A1, associated with familial digital clubbing, colon neoplasia, and NSAID resistance,” Cancer Prevention Research, vol. 7, no. 8, pp. 805–812, 2014. View at Publisher · View at Google Scholar
  59. R. Kumar, A.-C. Clerc, I. Gori et al., “Lipoxin A4 prevents the progression of de novo and established endometriosis in a mouse model by attenuating prostaglandin E2 production and estrogen signaling,” PLoS ONE, vol. 9, no. 2, Article ID e89742, 2014. View at Publisher · View at Google Scholar
  60. M. C. Keightley, K. J. Sales, and H. N. Jabbour, “PGF2α-F-prostanoid receptor signalling via ADAMTS1 modulates epithelial cell invasion and endothelial cell function in endometrial cancer,” BMC Cancer, vol. 10, article 488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. S. K. Banu, J. A. Arosh, P. Chapdelaine, and M. A. Fortier, “Expression of prostaglandin transporter in the bovine uterus and fetal membranes during pregnancy,” Biology of Reproduction, vol. 73, no. 2, pp. 230–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. J. A. Arosh, S. K. Banu, S. Kimmins, P. Chapdelaine, L. A. MacLaren, and M. A. Fortier, “Effect of interferon-τ on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2,” Endocrinology, vol. 145, no. 11, pp. 5280–5293, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. H. N. Jabbour, S. A. Milne, A. R. W. Williams, R. A. Anderson, and S. C. Boddy, “Expression of COX-2 and PGE synthase and synthesis of PGE2 in endometrial adenocarcinoma: a possible autocrine/paracrine regulation of neoplastic cell function via EP2/EP4 receptors,” British Journal of Cancer, vol. 85, no. 7, pp. 1023–1031, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Oral, D. L. Olive, and A. Arici, “The peritoneal environment in endometriosis,” Human Reproduction Update, vol. 2, no. 5, pp. 385–398, 1996. View at Publisher · View at Google Scholar · View at Scopus