Placenta
Volume 30, Issue 6 , Pages 501-506 , June 2009

NK Cells Detect Changes in Adaptive Immunity within Mouse Decidua from Gestation Day Eight

  • K. Hatta

      Affiliations

    • Department of Microbiology and Immunology, Queen's University, Botterell Hall, Room 813, 18 Stuart Street, Kingston, Ontario K7L 3N6, Canada
    • Corresponding Author InformationCorresponding author. Tel.: +1 613 533 6000x74917; fax: +1 613 533 6796.
  • ,
  • M.J. van den Heuvel

      Affiliations

    • Biomedical Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
  • ,
  • B.A. Croy

      Affiliations

    • Anatomy and Cell Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada

,Accepted 2 April 2009.

References 

  1. King A, Burrows T, Loke YW. Human uterine natural killer cells. Nat Immunol. 1996;15:41–52
  2. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol. 2002;2:656–663
  3. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev. 2006;214:161–185
  4. Carlino C, Stabile H, Morrone S, Bulla R, Soriani A, Agostinis C, et al. Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy. Blood. 2008;111:3108–3115
  5. Lynch L, Golden-Mason L, Eogan M, O'Herlihy C, O'Farrelly C. Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility?. Hum Reprod. 2007;22:919–926
  6. Kitaya K, Yamaguchi T, Honjo H. Central role of interleukin-15 in postovulatory recruitment of peripheral blood CD16(−) natural killer cells into human endometrium. J Clin Endocrinol Metab. 2005;90:2932–2940
  7. Stamper HB, Woodruff JJ. Lymphocyte homing into lymph nodes: in vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules. J Exp Med. 1976;144:828–833
  8. Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood. 2001;97:2727–2733
  9. Evans SS, Bain MD, Wang WC. Fever-range hyperthermia stimulates alpha4beta7 integrin-dependent lymphocyte-endothelial adhesion. Int J Hyperthermia. 2000;16:45–59
  10. Wang WC, Goldman LM, Schleider DM, Appenheimer MM, Subjeck JR, Repasky EA, et al. Fever-range hyperthermia enhances l-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol. 1998;160:961–969
  11. Burke SD, Dong H, Hazan AD, Croy BA. Aberrant endometrial features of pregnancy in diabetic NOD mice. Diabetes. 2007;56:2919–2926
  12. van den Heuvel MJ, Horrocks J, Bashar S, Hatta K, Burke S, Evans SS, et al. Periovulatory increases in tissue homing potential of circulating CD56(bright) cells are associated with fertile menstrual cycles. J Clin Endocrinol Metab. 2005;90:3606–3613
  13. 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 2 weeks after missed menses. Am J Reprod Immunol. 2008;59:90–98
  14. van den Heuvel MJ, Horrocks J, Bashar S, Taylor S, Burke S, Hatta K, et al. Menstrual cycle hormones induce changes in functional interactions between lymphocytes and decidual vascular endothelial cells. J Clin Endocrinol Metab. 2005;90:2835–2842
  15. Peralta CG, Han VK, Horrocks J, Croy BA, van den Heuvel MJ. CD56 bright cells increase expression of {alpha}4 integrin at ovulation in fertile cycles. J Leukoc Biol. 2008;84:1065–1074
  16. Chantakru S, Wang WC, van den Heuvel M, Bashar S, Simpson A, Chen Q, et al. Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones. J Immunol. 2003;171:4011–4019
  17. Miller MJ, Wei SH, Parker I, Cahalan MD. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science. 2002;296:1869–1873
  18. Cahalan MD, Parker I, Wei SH, Miller MJ. Two-photon tissue imaging: seeing the immune system in a fresh light. Nat Rev Immunol. 2002;2:872–880
  19. Miller MJ, Wei SH, Cahalan MD, Parker I. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc Natl Acad Sci U S A. 2003;100:2604–2609
  20. Kammerer U, Kruse A, Barrientos G, Arck PC, Blois SM. Role of dendritic cells in the regulation of maternal immune responses to the fetus during mammalian gestation. Immunol Invest. 2008;37:499–533
  21. Shakhar G, Lindquist RL, Skokos D, Dudziak D, Huang JH, Nussenzweig MC, et al. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol. 2005;6:707–714
  22. Ashkar AA, Croy BA. Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod. 1999;61:493–502
  23. Croy BA, Chapeau C, Reed N, Stewart IJ, Peel S. Is there an essential requirement for bone-marrow-derived cells at the fetomaternal interface during successful pregnancy? A study of pregnancies in immunodeficient mice. In:  Wegmann TG,  Gill TJ,  Nisbet-Brown E editor. Molecular and cellular immunology of the maternal fetal interface. New York: Oxford University Press; 1991;p. 168–188
  24. Hunt JS, Miller L, Vassmer D, Croy BA. Expression of the inducible nitric oxide synthase gene in mouse uterine leukocytes and potential relationships with uterine function during pregnancy. Biol Reprod. 1997;57:827–836
  25. Guimond MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med. 1998;187:217–223
  26. Chtanova T, Schaeffer M, Han SJ, van Dooren GG, Nollmann M, Herzmark P, et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity. 2008;29:487–496
  27. Cahalan MD, Parker I. Close encounters of the first and second kind: T–DC and T–B interactions in the lymph node. Semin Immunol. 2005;17:442–451
  28. Bousso P, Robey E. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol. 2003;4:579–585
  29. Hommel M, Kyewski B. Dynamic changes during the immune response in T cell-antigen-presenting cell clusters isolated from lymph nodes. J Exp Med. 2003;197:269–280
  30. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, et al. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol. 2003;162:887–896
  31. Kang SJ, Liang HE, Reizis B, Locksley RM. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity. 2008;29:819–833
  32. Croy BA, di Santo JP, Greenwood JD, Chantakru S, Ashkar AA. Transplantation into genetically alymphoid mice as an approach to dissect the roles of uterine natural killer cells during pregnancy – a review. Placenta. 2000;21(Suppl. A):S77–S80
  33. van den Heuvel MJ, Peralta CG, Hatta K, Han VK, Clark DA. Decline 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
  34. Xie X, He H, Colonna M, Seya T, Takai T, Croy BA. Pathways participating in activation of mouse uterine natural killer cells during pregnancy. Biol Reprod. 2005;73:510–518
  35. Paffaro VA, Bizinotto MC, Joazeiro PP, Yamada AT. Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta. 2003;24:479–488
  36. Kusakabe K, Okada T, Sasaki F, Kiso Y. Cell death of uterine natural killer cells in murine placenta during placentation and preterm periods. J Vet Med Sci. 1999;61:1093–1100
  37. Ye W, Zheng LM, Young JD, Liu CC. The involvement of interleukin (IL)-15 in regulating the differentiation of granulated metrial gland cells in mouse pregnant uterus. J Exp Med. 1996;184:2405–2410
  38. Oh MJ, Croy BA. A map of relationships between uterine natural killer cells and progesterone receptor expressing cells during mouse pregnancy. Placenta. 2008;29:317–323
  39. Sabatos CA, Doh J, Chakravarti S, Friedman RS, Pandurangi PG, Tooley AJ, et al. A synaptic basis for paracrine interleukin-2 signaling during homotypic T cell interaction. Immunity. 2008;29:238–248
  40. Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987;236:799–806
  41. Hoffman S, Edelman GM. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc Natl Acad Sci U S A. 1983;80:5762–5766
  42. Rutishauser U, Hoffman S, Edelman GM. Binding properties of a cell adhesion molecule from neural tissue. Proc Natl Acad Sci U S A. 1982;79:685–689

PII: S0143-4004(09)00112-X

doi: 10.1016/j.placenta.2009.04.001

Placenta
Volume 30, Issue 6 , Pages 501-506 , June 2009