Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2018, Article ID 7041342, 12 pages
https://doi.org/10.1155/2018/7041342
Research Article

The Increase of Circulating PD-1- and PD-L1-Expressing Lymphocytes in Endometriosis: Correlation with Clinical and Laboratory Parameters

1I Department of Gynecology, Medical University of Lublin, 16 Staszica Street, 20-081 Lublin, Poland
2Department of Clinical Immunology and Immunotherapy, Medical University of Lublin, 4a Chodzki Street, 20-093 Lublin, Poland
3Department of Pharmaceutical Microbiology with Laboratory for Microbiological Diagnostics, Medical University of Lublin, 1 Chodzki Street, 20-093 Lublin, Poland
4Augusta Kliniken Bochum, 26 Bergstrasse Street, 44791 Bochum, Germany

Correspondence should be addressed to Ewelina Grywalska; moc.liamg@akslawyrg.anilewe

Received 26 May 2018; Accepted 27 September 2018; Published 25 November 2018

Academic Editor: Carla Pagliari

Copyright © 2018 Monika Walankiewicz 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. D. Gupta, M. L. Hull, I. Fraser et al., “Endometrial biomarkers for the non-invasive diagnosis of endometriosis,” Cochrane Database of Systematic Reviews, vol. 4, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. L. C. Giudice and L. C. Kao, “Endometriosis,” The Lancet, vol. 364, no. 9447, pp. 1789–1799, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Sourial, N. Tempest, and D. K. Hapangama, “Theories on the pathogenesis of endometriosis,” International Journal of Reproductive Medicine, vol. 2014, Article ID 179515, 9 pages, 2014. View at Publisher · View at Google Scholar
  4. P. Viganò, F. Parazzini, E. Somigliana, and P. Vercellini, “Endometriosis: epidemiology and aetiological factors,” Best Practice & Research Clinical Obstetrics & Gynaecology, vol. 18, no. 2, pp. 177–200, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. D. L. Olive and E. A. Pritts, “Treatment of endometriosis,” New England Journal of Medicine, vol. 345, no. 4, pp. 266–275, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. B. S. Verkauf, “Incidence, symptoms, and signs of endometriosis in fertile and infertile women,” The Journal of the Florida Medical Association, vol. 74, no. 9, pp. 671–675, 1987. View at Google Scholar
  7. C. Bulletti, M. E. Coccia, S. Battistoni, and A. Borini, “Endometriosis and infertility,” Journal of Assisted Reproduction and Genetics, vol. 27, no. 8, pp. 441–447, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. M. L. Macer and H. S. Taylor, “Endometriosis and infertility: a review of the pathogenesis and treatment of endometriosis-associated infertility,” Obstetrics and Gynecology Clinics of North America, vol. 39, no. 4, pp. 535–549, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. V. A. Akande, L. P. Hunt, D. J. Cahill, and J. M. Jenkins, “Differences in time to natural conception between women with unexplained infertility and infertile women with minor endometriosis,” Human Reproduction, vol. 19, no. 1, pp. 96–103, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. J. L. Herington, K. L. Bruner-Tran, J. A. Lucas, and K. G. Osteen, “Immune interactions in endometriosis,” Expert Review of Clinical Immunology, vol. 7, no. 5, pp. 611–626, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Agostinis, S. Zorzet, R. de Leo, G. Zauli, F. de Seta, and R. Bulla, “The combination of N-acetyl cysteine, alpha-lipoic acid, and bromelain shows high anti-inflammatory properties in novel in vivo and in vitro models of endometriosis,” Mediators of Inflammation, vol. 2015, Article ID 918089, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. Bedaiwy, T. Falcone, R. K. Sharma et al., “Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial,” Human Reproduction, vol. 17, no. 2, pp. 426–431, 2002. View at Publisher · View at Google Scholar
  13. Y. Yu-Rice, S. L. Edassery, N. Urban et al., “Selenium-Binding Protein 1 (SBP1) autoantibodies in ovarian disorders and ovarian cancer,” Reproduction, vol. 153, no. 3, pp. 277–284, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Okazaki and T. Honjo, “The PD-1–PD-L pathway in immunological tolerance,” Trends in Immunology, vol. 27, no. 4, pp. 195–201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Nishimura, Y. Agata, A. Kawasaki et al., “Developmentally regulated expression of the PD-1 protein on the surface of double-negative (CD4–CD8–) thymocytes,” International Immunology, vol. 8, no. 5, pp. 773–780, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Ishida, Y. Agata, K. Shibahara, and T. Honjo, “Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death,” The EMBO Journal, vol. 11, no. 11, pp. 3887–3895, 1992. View at Publisher · View at Google Scholar
  17. R. K. Dinesh, B. H. Hahn, and R. P. Singh, “PD-1, gender, and autoimmunity,” Autoimmunity Reviews, vol. 9, no. 8, pp. 583–587, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. L. R. Finger, J. Pu, R. Wasserman et al., “The human PD-1 gene: complete cDNA, genomic organization, and developmentally regulated expression in B cell progenitors,” Gene, vol. 197, no. 1-2, pp. 177–187, 1997. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Nielsen, L. Ohm-Laursen, T. Barington, S. Husby, and S. T. Lillevang, “Alternative splice variants of the human PD-1 gene,” Cellular Immunology, vol. 235, no. 2, pp. 109–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. J. L. Riley, “PD-1 signaling in primary T cells,” Immunological Reviews, vol. 229, no. 1, pp. 114–125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Dai, R. Jia, X. Zhang, Q. Fang, and L. Huang, “The PD-1/PD-Ls pathway and autoimmune diseases,” Cellular Immunology, vol. 290, no. 1, pp. 72–79, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Agata, A. Kawasaki, H. Nishimura et al., “Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes,” International Immunology, vol. 8, no. 5, pp. 765–772, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Baecher-Allan, J. A. Brown, G. J. Freeman, and D. A. Hafler, “CD4+ CD25+ regulatory cells from human peripheral blood express very high levels of CD25 ex vivo,” Novartis Foundation Symposium, vol. 252, pp. 67–91, 2008. View at Publisher · View at Google Scholar
  24. M. E. Keir, M. J. Butte, G. J. Freeman, and A. H. Sharpe, “PD-1 and its ligands in tolerance and immunity,” Annual Review of Immunology, vol. 26, no. 1, pp. 677–704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. L. V. Riella, A. M. Paterson, A. H. Sharpe, and A. Chandraker, “Role of the PD-1 pathway in the immune response,” American Journal of Transplantation, vol. 12, no. 10, pp. 2575–2587, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Jing, M. Li, Y. Zhang et al., “PD-1/PD-L1 blockades in non-small-cell lung cancer therapy,” OncoTargets and Therapy, vol. 9, pp. 489–502, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Bartosińska, E. Zakrzewska, D. Raczkiewicz et al., “Suppressed programmed death 1 expression on CD4+ and CD8+ T cells in psoriatic patients,” Mediators of Inflammation, vol. 2017, Article ID 5385102, 8 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  28. L. M. Francisco, P. T. Sage, and A. H. Sharpe, “The PD-1 pathway in tolerance and autoimmunity,” Immunological Reviews, vol. 236, no. 1, pp. 219–242, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Nurieva, S. Thomas, T. Nguyen et al., “T-cell tolerance or function is determined by combinatorial costimulatory signals,” The EMBO Journal, vol. 25, no. 11, pp. 2623–2633, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Chemnitz, R. V. Parry, K. E. Nichols, C. H. June, and J. L. Riley, “SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation,” Journal of Immunology, vol. 173, no. 2, pp. 945–954, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Grywalska, I. Smarz-Widelska, E. Krasowska-Zajac et al., “The PD-1/PD-L1 inhibitory pathway is altered in primary glomerulonephritides,” Archivum Immunologiae et Therapiae Experimentalis, vol. 66, no. 2, pp. 133–143, 2017. View at Publisher · View at Google Scholar · View at Scopus
  32. X. Chen, D. Fosco, D. E. Kline et al., “PD-1 regulates extrathymic regulatory T-cell differentiation,” European Journal of Immunology, vol. 44, no. 9, pp. 2603–2616, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. T. S. Lim, V. Chew, J. L. Sieow et al., “PD-1 expression on dendritic cells suppresses CD8+ T cell function and antitumor immunity,” OncoImmunology, vol. 5, no. 3, article e1085146, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. J. T. McKay, R. P. Egan, R. D. Yammani et al., “PD-1 suppresses protective immunity to Streptococcus pneumoniae through a B cell-intrinsic mechanism,” Journal of Immunology, vol. 194, no. 5, pp. 2289–2299, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. American Society for Reproductive, “Revised American Society for Reproductive Medicine classification of endometriosis: 1996,” Fertility and Sterility, vol. 67, no. 5, pp. 817–821, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Sakaguchi, T. Yamaguchi, T. Nomura, and M. Ono, “Regulatory T cells and immune tolerance,” Cell, vol. 133, no. 5, pp. 775–787, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. A. D. Salama, T. Chitnis, J. Imitola et al., “Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis,” The Journal of Experimental Medicine, vol. 198, no. 1, pp. 71–78, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. E. Latchman, S. C. Liang, Y. Wu et al., “PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 29, pp. 10691–10696, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Nishimura, M. Nose, H. Hiai, N. Minato, and T. Honjo, “Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor,” Immunity, vol. 11, no. 2, pp. 141–151, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Okazaki, Y. Iwai, and T. Honjo, “New regulatory co-receptors: inducible co-stimulator and PD-1,” Current Opinion in Immunology, vol. 14, no. 6, pp. 779–782, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. W. P. Dmowski, H. M. Gebel, and D. P. Braun, “The role of cell-mediated immunity in pathogenesis of endometriosis,” Acta Obstetricia et Gynecologica Scandinavica. Supplement, vol. 159, pp. 7–14, 1994. View at Google Scholar
  42. V. H. Eisenberg, M. Zolti, and D. Soriano, “Is there an association between autoimmunity and endometriosis?” Autoimmunity Reviews, vol. 11, no. 11, pp. 806–814, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. S. G. Pasoto, M. S. Abrao, V. S. T. Viana, C. Bueno, E. P. Leon, and E. Bonfa, “Endometriosis and systemic lupus erythematosus: a comparative evaluation of clinical manifestations and serological autoimmune phenomena,” American Journal of Reproductive Immunology, vol. 53, no. 2, pp. 85–93, 2005. View at Publisher · View at Google Scholar
  44. S.-C. Lin, J.-H. Yen, J.-J. Tsai et al., “Association of a programmed death 1 gene polymorphism with the development of rheumatoid arthritis, but not systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 50, no. 3, pp. 770–775, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Wang, P. Hu, J. Yang, G. Shen, and X. Wu, “The effects of PDL-Ig on collagen-induced arthritis,” Rheumatology International, vol. 31, no. 4, pp. 513–519, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Wan, H. Nie, A. Liu et al., “Aberrant regulation of synovial T cell activation by soluble costimulatory molecules in rheumatoid arthritis,” The Journal of Immunology, vol. 177, no. 12, pp. 8844–8850, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Kobayashi, S. Kawano, S. Hatachi et al., “Enhanced expression of programmed death-1 (PD-1)/PD-L1 in salivary glands of patients with Sjögren’s syndrome,” The Journal of Rheumatology, vol. 32, no. 11, pp. 2156–2163, 2005. View at Google Scholar
  48. V. Gołabek and T. Woźniakowska-Gesicka, “Role of the PD-1/PD-L1 pathway in immunopathology of HBV infection as the chance on the new therapeutic strategy,” Przegla̧d Epidemiologiczny, vol. 64, no. 4, pp. 485–489, 2010. View at Google Scholar
  49. M. R. Zamani, F. A. Asbagh, A. H. Massoud, A. Salmaninejad, A. Massoud, and N. Rezaei, “Association between a PD-1 gene polymorphism and antisperm antibody-related infertility in Iranian men,” Journal of Assisted Reproduction and Genetics, vol. 32, no. 1, pp. 103–106, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Hamanishi, M. Mandai, T. Ikeda et al., “Safety and antitumor activity of anti-PD-1 antibody, Nivolumab, in patients with platinum-resistant ovarian cancer,” Journal of Clinical Oncology, vol. 33, no. 34, pp. 4015–4022, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. V. Heong, N. Ngoi, and D. S. P. Tan, “Update on immune checkpoint inhibitors in gynecological cancers,” Journal of Gynecologic Oncology, vol. 28, no. 2, article e20, 2017. View at Publisher · View at Google Scholar · View at Scopus
  52. S. L. Gaillard, A. A. Secord, and B. Monk, “The role of immune checkpoint inhibition in the treatment of ovarian cancer,” Gynecologic Oncology Research and Practice, vol. 3, no. 1, article 11, 2016. View at Publisher · View at Google Scholar
  53. P. A. Ott, Y.-J. Bang, D. Berton-Rigaud et al., “Safety and antitumor activity of Pembrolizumab in advanced programmed death ligand 1-positive endometrial cancer: results from the KEYNOTE-028 study,” Journal of Clinical Oncology, vol. 35, no. 22, pp. 2535–2541, 2017. View at Publisher · View at Google Scholar · View at Scopus
  54. A. N. Fader, L. A. Diaz, D. K. Armstrong et al., “Preliminary results of a phase II study: PD-1 blockade in mismatch repair-deficient, recurrent or persistent endometrial cancer,” Gynecologic Oncology, vol. 141, pp. 206-207, 2016. View at Publisher · View at Google Scholar
  55. K. A. Burns, K. F. Rodriguez, S. C. Hewitt, K. S. Janardhan, S. L. Young, and K. S. Korach, “Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model,” Endocrinology, vol. 153, no. 8, pp. 3960–3971, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. Q. Xue, Z. Lin, Y.-H. Cheng et al., “Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis,” Biology of Reproduction, vol. 77, no. 4, pp. 681–687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Trukhacheva, Z. Lin, S. Reierstad, Y.-H. Cheng, M. Milad, and S. E. Bulun, “Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis,” The Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 2, pp. 615–622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. M. J. Polanczyk, C. Hopke, A. A. Vandenbark, and H. Offner, “Estrogen-mediated immunomodulation involves reduced activation of effector T cells, potentiation of Treg cells, and enhanced expression of the PD-1 costimulatory pathway,” Journal of Neuroscience Research, vol. 84, no. 2, pp. 370–378, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. C. Wang, B. Dehghani, Y. Li, L. J. Kaler, A. A. Vandenbark, and H. Offner, “Oestrogen modulates experimental autoimmune encephalomyelitis and interleukin-17 production via programmed death 1,” Immunology, vol. 126, no. 3, pp. 329–335, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. I. M. Matalliotakis, I. Athanassakis, A. G. Goumenou et al., “The possible anti-inflammatory role of circulating human leukocyte antigen levels in women with endometriosis after treatment with danazol and leuprorelin acetate depot,” Mediators of Inflammation, vol. 10, no. 2, pp. 75–80, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. F. Barra, C. Scala, V. Mais, S. Guerriero, and S. Ferrero, “Investigational drugs for the treatment of endometriosis, an update on recent developments,” Expert Opinion on Investigational Drugs, vol. 27, no. 5, pp. 445–458, 2018. View at Publisher · View at Google Scholar · View at Scopus