Reproductive BioMedicine Online
Volume 21, Issue 6 , Pages 750-756 , December 2010

Possible role of natural killer and natural killer T-like cells in implantation failure after IVF

  • Eva Miko

      Affiliations

    • Department of Medical Microbiology and Immunology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Zoltan Manfai

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Matyas Meggyes

      Affiliations

    • Department of Medical Microbiology and Immunology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Aliz Barakonyi

      Affiliations

    • Department of Medical Microbiology and Immunology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Ferenc Wilhelm

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Akos Varnagy

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Jozsef Bodis

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Zsolt Illes

      Affiliations

    • Department of Neurology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Julia Szekeres-Bartho

      Affiliations

    • Department of Medical Microbiology and Immunology, University of Pecs, Medical School, Pecs, Hungary
  • ,
  • Laszlo Szereday

      Affiliations

    • Department of Medical Microbiology and Immunology, University of Pecs, Medical School, Pecs, Hungary
    • Corresponding Author InformationCorresponding author.

Received 11 March 2010 ,Revised 23 July 2010 ,Accepted 27 July 2010.

References 

  1. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods. 2004;294:15–22
  2. Andzelm MM, Chen X, Krzewski K, Orange JS, Strominger JL. Myosin IIA is required for cytolytic granule exocytosis in human NK cells. J. Exp. Med. 2007;204:2285–2291
  3. Aoki K, Kajiura S, Matsumoto Y, et al. Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet. 1995;345:1340–1342
  4. Beer AE, Kwak JY, Ruiz JE. Immunophenotypic profiles of peripheral blood lymphocytes in women with recurrent pregnancy losses and in infertile women with multiple failed in vitro fertilization cycles. Am. J. Reprod. Immunol. 1996;35:376–382
  5. Borzychowski AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur. J. Immunol. 2005;35:3054–3063
  6. Carosella ED, HoWangYin KY, Favier B, LeMaoult J. HLA-G-dependent suppressor cells: diverse by nature, function, and significance. Hum. Reprod. 2008;69:700–707
  7. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22:633–640
  8. Coulam CB, Roussev RG. Correlation of NK cell activation and inhibition markers with NK cytotoxicity among women experiencing immunologic implantation failure after in vitro fertilization and embryo transfer. J. Assist. Reprod. Genet. 2003;20:58–62
  9. Coulam CB, Goodman C, Roussev RG, Thomason EJ, Beaman KD. Systemic CD56+ cells can predict pregnancy outcome. Am. J. Reprod. Immunol. 1995;33:40–46
  10. Croy BA, He H, Esadeg S, et al. Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction. 2003;126:149–160
  11. Hiby SE, Walker JJ, O’shaughnessy KM, et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 2004;200:957–965
  12. Hunt JS, Langat DL. HLA-G: a human pregnancy-related immunomodulator. Curr. Opin. Pharmacol. 2009;9:462–469
  13. Hviid TV. HLA-G in human reproduction: aspects of genetics, function and pregnancy complications. Hum. Reprod. Update. 2006;12:209–232
  14. Ishitani A, Sageshima N, Hatake K. The involvement of HLA-E and -F in pregnancy. J. Reprod. Immunol. 2006;69:101–113
  15. King K, Smith S, Chapman M, Sacks G. Detailed analysis of peripheral blood natural killer (NK) cells in women with recurrent miscarriage. Hum. Reprod. 2009;(Epub ahead of print)
  16. Koopman LA, Kopcow HD, Rybalov B, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 2003;198:1201–1212
  17. Kronenberg M, Gapin L. The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2002;2:557–568
  18. Kwak-Kim J, Gilman-Sachs A. Clinical implication of natural killer cells and reproduction. Am. J. Reprod. Immunol. 2008;59:388–400
  19. Lanier LL. NK cell recognition. Annu. Rev. Immunol. 2005;23:225–274
  20. Lash GE, Schiessl B, Kirkley M, et al. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc. Biol. 2006;80:572–580
  21. Li XF, Charnock-Jones DS, Zhang E, et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2001;86:1823–1834
  22. Marzi M, Vigano A, Trabattoni D, et al. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin. Exp. Immunol. 1996;106:127–133
  23. Monney L, Sabatos CA, Gaglia JL, et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature. 2002;415:536–541
  24. Ntrivalas EI, Kwak-Kim JY, Gilman-Sachs A, et al. Status of peripheral blood natural killer cells in women with recurrent spontaneous abortions and infertility of unknown aetiology. Hum. Repord. 2001;16:855–861
  25. Ntrivalas EI, Bowser CR, Kwak-Kim J, Beaman KD, Gilman-Sachs A. Expression of killer immunoglobulin-like receptors on peripheral blood NK cell subsets of women with recurrent spontaneous abortions or implantation failures. Am. J. Reprod. Immunol. 2005;53:215–221
  26. Quenby S, Farquharson R. Uterine natural killer cells, implantation failure and recurrent miscarriage. Reprod. Biomed. Online. 2006;13:24–28
  27. Raghupathy R, Makhseed M, Azizieh F, Omu A, Gupta M, Farhat R. Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Hum. Reprod. 2000;15:713–718
  28. Raulet DH. Missing self recognition and self tolerance of natural killer (NK) cells. Semin. Immunol. 2006;18:145–150
  29. Saito S, Sakai M, Sasaki Y, Tanebe K, Tsuda H, Michimata T. Quantitative analysis of peripheral blood Th0, Th1, Th2 and the Th1:Th2 cell ratio during normal human pregnancy and preeclampsia. Clin. Exp. Immunol. 1999;117:550–555
  30. Santoni A, Carlino C, Gismondi A. Uterine NK cell development, migration and function. Reprod. Biomed. Online. 2008;16:202–210
  31. Sargent IL, Borychowski AM, Redman CW. Immunoregulation in normal pregnancy and pre-eclampsia: an overview. Reprod. Biomed. Online. 2006;13:680–688
  32. Szekeres-Bartho J. Regulation of NK cell cytotoxicity during pregnancy. Reprod. Biomed. Online. 2008;16:211–217
  33. Szereday L, Spath P, Szekeres-Bartho J. Natural killer cell activity and cytokine production after in vitro immunoglobulin treatment of lymphocytes derived from pregnant women with or without risk for spontaneous abortion. Am. J. Reprod. Immunol. 1999;42:282–287
  34. Thum MY, Bhaskaran S, Abdalla HI, et al. An increase in the absolute count of CD56dimCD16+CD69+ NK cells in the peripheral blood is associated with a poorer IVF treatment and pregnancy outcome. Hum. Reprod. 2004;19:2395–2400
  35. Thum MY, Bhaskaran S, Bansal AS, et al. Simple enumerations of peripheral blood natural killer (CD56+ NK) cells, B cells and T cells have no predictive value in IVF treatment outcome. Hum. Reprod. 2005;20:1272–1276
  36. van den Heuvel MJ, Peralta CG, Hatta K, Han VK, Clark DA. Line in number of elevated blood CD3(+) CD56(+) NKT cells in response to intravenous immunoglobulin treatment correlates with successful pregnancy. Am. J. Reprod. Immunol. 2007;58:447–459
  37. van den Heuvel MJ, Hatta K, Peralta CG, Han VK, Clark DA. CD56+ cells are recruited to the uterus in two waves: at ovulation and during the first 2weeks after missed menses. Am. J. Reprod. Immunol. 2008;59:90–98
  38. Varla-Leftherioti M, Spyropoulou-Vlachou M, Niokou D, et al. Natural killer (NK) cell receptors’ repertoire in couples with recurrent spontaneous abortions. Am. J. Reprod. Immunol. 2003;49:183–191
  39. Varla-Leftherioti M, Spyropoulou-Vlachou M, Keramitsoglou T, et al. Lack of the appropriate natural killer cell inhibitory receptors in women with spontaneous abortion. Hum. Immunol. 2005;66:65–71
  40. Winger EE, Reed JL, Ashoush S, Ahuja S, El-Toukhy T, Taranissi M. Treatment with adalimumab (Humira) and intravenous immunoglobulin improves pregnancy rates in women undergoing IVF. Am. J. Reprod. Immunol. 2009;61:113–120
  41. Yokoyama WM, Riley JK. NK cells and their receptors. Reprod. Biomed. Online. 2008;16:173–191

 Laszlo Szereday, MD, PhD, received his medical training at the University of Pecs, Medical School, Hungary. After a postdoctoral fellowship at Joslin Diabetes Center, Harvard Medical School, he is now an associate professor at the Department of Medical Microbiology and Immunology, University of Pecs. He was awarded with the Habilitation in the same establishment. His main research interest is reproductive immunology and immunological background of infectious diseases.

PII: S1472-6483(10)00510-9

doi: 10.1016/j.rbmo.2010.07.012

Reproductive BioMedicine Online
Volume 21, Issue 6 , Pages 750-756 , December 2010