Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells

European Journal of Immunology

Volumn 35, Issue 10, 2005, Pages 3054-3063

  Borzychowski, Angela M ^a,b   Croy, B Anne ^c   Chan, W Ling ^d   Redman, Christopher W G ^a   Sargent, Ian L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF GUELPH   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Human pregnancy; IL 18R; NK cells; Pre eclampsia; ST2L

Indexed keywords

INTERLEUKIN 18;

ADULT; ARTICLE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; FEMALE; FLOW CYTOMETRY; GESTATION PERIOD; HELPER CELL; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; NATURAL KILLER CELL; PERIPHERAL LYMPHOCYTE; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; TH1 CELL; TH2 CELL; THIRD TRIMESTER PREGNANCY;

ADULT; FEMALE; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-18; KILLER CELLS, NATURAL; MEMBRANE PROTEINS; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, CELL SURFACE; TH1 CELLS; TH2 CELLS;

EID: 27644450047     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425929     Document Type: Article

References (55)

1. Moffett-King, A., Natural killer cells and pregnancy. Nat. Rev. Immunol. 2002. 2: 656-663.
2. Brosens, I. A., Robertson, W. B. and Dixon, H. G., The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet. Gynecol. Annu. 1972. 1: 177-191.
3. Haller, H., Radillo, O., Rukavina, D., Tedesco, F., Candussi, G., Petrovic, O. and Randic, L., An immunohistochemical study of leucocytes in human endometrium, first and third trimester basal decidua. J. Reprod. Immunol. 1993. 23: 41-49.
4. Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y. P., Skepper, J. N. and Burton, G. J., Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 2000. 157: 2111-2122.
5. Wegmann, T. G., Lin, H., Guilbert, L. and Mosmann, T. R., Bidirectional cytokine interactions in the maternal-foetal relationship: is successful pregnancy a Th2 phenomenon? Immunol. Today 1993. 14: 353-356.
6. Zenclussen, A. C., Fest, S., Busse, P., Joachim, R., Klapp, B. F. and Arck, P. C., Questioning the Th1/Th2 paradigm in reproduction: peripheral levels of IL-12 are down-regulated in miscarriage patients. Am. J. Reprod. Immunol. 2002. 48: 245-251.
7. Chaouat, G., Innately moving away from the Th1/Th2 paradigm in pregnancy. Clin. Exp. Immunol. 2003. 131: 393-395.
8. Hiby, S. E., Walker, J. J., O'Shaughnessy, K. M., Redman, C. W., Carrington, M., Trowsdale, J. and Moffett, A., Combinations of maternal KIR and foetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 2004. 200: 957-965.
9. Redman, C. W. and Sargent, I. L., Pre-eclampsia, the placenta and the maternal systemic inflammatory response - a review. Placenta 2003. 24 Suppl A: S21-S27.
10. Sunderland, C. A., Naiem, M., Mason, D. Y., Redman, C. W. and Stirrat, G. M., The expression of major histocompatibility antigens by human chorionic villi. J. Reprod. Immunol. 1981. 3: 323-331.
11. Ashkar, A. A., Di Santo, J. P. and Croy, B. A., Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal routine pregnancy. J. Exp. Med. 2000. 192: 259-270.
12. - cells in total natural killer cells as an indication of fertility and infertility. Fertil. Steril. 2003. 80 Suppl 2: 691-697.
13. Redman, C. W. and Sargent, I. L., Latest advances in understanding preeclampsia. Science 2005. 308: 1592-1594.
14. Redman, C. W. and Sargent, I. L., The pathogenesis of pre-eclampsia. Gynecol. Obstet. Fertil. 2001. 29: 518-522.
15. Sacks, G. P., Studena, K., Sargent, I. L. and Redman, C. W., Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am. J. Obstet. Gynecol. 1998. 179: 80-86.
16. + T cells into subpopulations with distinct cytokine profiles. J. Immunol. 1995. 155: 2928-2937.
17. Carter, L. L. and Dutton, R. W., Relative perform- and Fas-mediated lysis in T1 and T2 CD8 effector populations. J. Immunol. 1995. 155: 1028-1031.
18. Peritt, D., Robertson, S., Gri, G., Showe, L., Aste-Amezaga, M. and Trinchieri, G., Differentiation of human NK cells into NK1 and NK2 subsets. J. Immunol. 1998. 161: 5821-5824.
19. Deniz, G., Akdis, M., Aktas, E., Blaser, K. and Akdis, C. A., Human NK1 and NK2 subsets determined by purification of IFN-gamma-secreting and IFN-gamma-nonsecreting NK cells. Eur. J. Immunol. 2002. 32: 879-884.
20. Chan, W. L., Pejnovic, N., Lee, C. A. and Al-Ali, N. A., Human IL-18 receptor and ST2L are stable and selective markers for the respective type 1 and type 2 circulating lymphocytes. J. Immunol. 2001. 167: 1238-1244.
21. Cooper, M. A., Fehniger, T. A. and Caligiuri, M. A., The biology of human natural killer-cell subsets. Trends Immunol. 2001. 22: 633-640.
22. Kadowaki, N., Antonenko, S., Ho, S., Rissoan, M. C., Soumelis, V., Porcelli, S. A., Lanier, L. L. and Liu, Y. J., Distinct cytokine profiles of neonatal natural killer T cells after expansion with subsets of dendritic cells. J. Exp. Med. 2001. 193: 1221-1226.
23. Marzi, M., Vigano, A., Trabattoni, D., Villa, M. L., Salvaggio, A., Clerici, E. and Clerici, M., Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin. Exp. Immunol. 1996. 106: 127-133.
24. Saito, S., Sakai, M., Sasaki, Y., Tanebe, K., Tsuda, H. and 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.
25. Saito, S., Umekage, H., Sakamoto, Y., Sakai, M., Tanebe, K., Sasaki, Y. and Morikawa, H., Increased T-helper-1-type immunity and decreased Thelper-2-type immunity in patients with preeclampsia. Am. J. Reprod. Immunol. 1999. 41: 297-306.
26. Darmochwal-Kolarz, D., Leszczynska-Gorzelak, B., Rolinski, J. and Oleszczuk, J., T helper 1- and T helper 2-type cytokine imbalance in pregnant women with pre-eclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 1999. 86: 165-170.
27. Rein, D. T., Schondorf, T., Gohring, U. J., Kurbacher, C. M., Pinto, I., Breidenbach, M., Mallmann, P., Kolhagen, H. and Engel, H., Cytokine expression in peripheral blood lymphocytes indicates a switch to T(helper) cells in patients with preeclampsia. J. Reprod. Immunol. 2002. 54: 133-142.
28. Xu, D., Chan, W. L., Leung, B. P., Hunter, D., Schulz, K., Carter, R. W., McInnes, I. B., Robinson, J. H. and Liew, F. Y., Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J. Exp. Med. 1998. 188: 1485-1492.
29. Xu, D., Chan, W. L., Leung, B. P., Huang, F., Wheeler, R., Piedrafita, D., Robinson, J. H. and Liew, F. Y., Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J. Exp. Med. 1998. 187: 787-794.
30. Chan, W. L., Pejnovic, N., Liew, T. V., Lee, C. A., Groves, R. and Hamilton, H., NKT cell subsets in infection and inflammation. Immunol. Lett. 2003. 85: 159-163.
31. Nakanishi, K., Yoshimoto, T., Tsutsui, H. and Okamura, H., Interleukin-18 regulates both Th1 and Th2 responses. Annu. Rev. Immunol. 2001. 19: 423-474.
32. Brint, E. K., Fitzgerald, K. A., Smith, P., Coyle, A. J., Gutierrez-Ramos, J. C., Fallon, P. G. and O'Neill, L. A., Characterization of signaling pathways activated by the interleukin 1 (IL-1) receptor homologue T1/ST2. A role for Jun N-terminal kinase in IL-4 induction. J. Biol. Chem. 2002. 277: 49205-49211.
33. Brint, E. K., Xu, D., Liu, H., Dunne, A., McKenzie, A. N., O'Neill, L. A. and Liew, F. Y., ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat. Immunol. 2004. 5: 373-379.
34. Darmochwal-Kolarz, D., Rolinski, J., Leszczynska-Goarzelak, B. and Oleszczuk, J., The expressions of intracellular cytokines in the lymphocytes of preeclamptic patients. Am. J. Reprod. Immunol. 2002. 48: 381-386.
35. Sakai, M., Tsuda, H., Tanebe, K., Sasaki, Y. and Saito, S., Interleukin-12 secretion by peripheral blood mononuclear cells is decreased in normal pregnant subjects and increased in preeclamptic patients. Am. J. Reprod. Immunol. 2002. 47: 91-97.
36. Reinhard, G., Noll, A., Schlebusch, H., Mallmann, P. and Ruecker, A. V., Shifts in the TH1/TH2 balance during human pregnancy correlate with apoptotic changes. Biochem. Biophys. Res. Commun. 1998. 245: 933-938.
37. Veenstra van Nieuwenhoven, A. L., Bouman, A., Moes, H., Heineman, M. J., de Leij, L. F., Santema, J. and Faas, M. M., Cytokine production in natural killer cells and lymphocytes in pregnant women compared with women in the follicular phase of the ovarian cycle. Fertil. Steril. 2002. 77: 1032-1037.
38. Redman, C. W., Sacks, G. P. and Sargent, I. L., Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am. J. Obstet. Gynecol. 1999. 180: 499-506.
39. King, A., Burrows, T., Verma, S., Hiby, S. and Loke, Y. W., Human uterine lymphocytes. Hum. Reprod. Update 1998. 4: 480-485.
40. Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E. and Caligiuri, M. A., Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 2001. 97: 3146-3151.
41. Hammond, K. J. and Godfrey, D. I., NKT cells: potential targets for autoimmune disease therapy? Tissue Antigens 2002. 59: 353-363.
42. Bendelac, A., Rivera, M. N., Park, S. H. and Roark, J. H., Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 1997. 15: 535-562.
43. Sandberg, J. K., Bhardwaj, N. and Nixon, D. F., Dominant effector memory characteristics, capacity for dynamic adaptive expansion, and sex bias in the innate Valpha24 NKT cell compartment. Eur. J. Immunol. 2003. 33: 588-596.
44. Brigl, M. and Brenner, M. B., CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 2004. 22: 817-890.
45. + T cells produce large amounts of IL-4 and IFN-gamma upon activation by anti-CD3 or CD1. J. Immunol. 1997 159: 2240-2249.
46. Ami, K., Ohkawa, T., Koike, Y., Sato, K., Hahn, Y., Iwai, T., Seki, S. and Hiraide, H., Activation of human T cells with NK cell markers by staphylococcal enterotoxin A via IL-12 but not via IL-18. Clin. Exp. Immunol. 2002. 128: 453-459.
47. Walker, D., Jason, J., Wallace, K., Slaughter, J., Whatley, V., Han, A., Nwanyanwu, O. C. et al., Spontaneous cytokine production and its effect on induced production. Clin. Diagn. Lab. Immunol. 2002. 9: 1049-1056.
48. Oki, S., Chiba, A., Yamamura, T. and Miyake, S., The clinical implication and molecular mechanism of preferential IL-4 production by modified glycolipid-stimulated NKT cells. J. Clin. Invest. 2004. 113: 1631-1640.
49. + NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood 2004. 103: 383-389.
50. Kammerer, U., Eggert, A. O., Kapp, M., McLellan, A. D., Geijtenbeek, T. B., Dietl, J., van Kooyk, Y. and Kampgen, E., 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.
51. Sacks, G. P., Redman, C. W. and Sargent, I. L., Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells. Clin. Exp. Immunol. 2003. 131: 490-497.
52. Takeda, K., Kaisho, T. and Akira, S., Toll-like receptors. Annu. Rev. Immunol. 2003. 21: 335-376.
53. Aluvihare, V. R., Kallikourdis, M. and Betz, A. G., Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004. 5: 266-271.
54. + regulatory T-cell subset. Immunology 2004. 112: 38-43.
55. Kunikata, T., Torigoe, K., Ushio, S., Okura, T., Ushio, C., Yamauchi, H., Ikeda, M., Ikegami, H. and Kurimoto, M., Constitutive and induced IL-18 receptor expression by various peripheral blood cell subsets as determined by anti-hIL-18R monoclonal antibody. Cell. Immunol. 1998, 189: 135-143.