Emerging role of uterine natural killer cells in establishing pregnancy

Iranian Journal of Immunology

Volumn 5, Issue 2, 2008, Pages 71-81

  Kumar, Vijay ^a   Medhi, Bikash ^b  

^a PANJAB UNIVERSITY   (India)

^b POSTGRADUATE INSTITUTE OF MEDICAL EDUCATION AND RESEARCH   (India)

Author keywords

Decidua; Implantation; NK cells; Pregnancy; Trophoblasts

Indexed keywords

STEROID RECEPTOR;

BLASTOCYST; CELL FUNCTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DECIDUA; HIGH RISK PREGNANCY; HLA SYSTEM; HORMONAL REGULATION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; MOTHER FETUS RELATIONSHIP; NATURAL KILLER CELL; PLACENTA; PREGNANCY; PROTEIN EXPRESSION; REVIEW; TH1 CELL; TH2 CELL; TROPHOBLAST; UTERUS;

EID: 45349101911     PISSN: 17351383     EISSN: 1735367X     Source Type: Journal    
DOI: None     Document Type: Review

References (74)

1. Head JR, Billingham RE. Immunobiological aspects of the maternal feto-placental relationship. In Lachmann PJ, Peters DK eds. Clinical aspects of immunology, Volume 1. London: Blackwell Scientific Publications, 1983 p 243-82.
2. Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today 1993; 14: 353-56.
3. Vince GS, Johnson PM. Is there a Th2 bias in human pregnancy? J Reprod Immunol. 1996; 32: 101-4.
4. Mellor AL, Chandler P, Lee GK, Johnson T, Keskin DB, Lee J et al. Indoleamine 2,3-dioxygenase, immunosuppression and pregnancy. J Reprod Immunol. 2002; 57:143-50.
5. Goldman-Wohl D, Yagel S. NK cells and pre-eclampsia. Repro Biomed Online. 2008; 16: 227-31.
6. Bulmer J, Lash G. Human uterine natural killer cells: a reappraisal. Mol Immunol. 2005; 42: 511-21.
7. Sacks G, Sargent I, Redman C. An innate view of human pregnancy. Immunol Tod. 1999; 20: 114-8.
8. King A, Burrows T, verma S, Hiby S, Loke YW. Human uterine lymphocytes. Human Reprod Update. 1998; 4: 480-5.
9. Santoni A, Carlino C, Stabile H, Gismondi A. Mechanisms underlying recruitment and accumulation of decidual NK cells in uterus during pregnancy. Am J Reprod Immunol. 2008; 59: 417-24.
10. Hanna J, Wald O, Goldman-Wohl D, Prus D, Markel G, Gazit R et al. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood. 2003; 102:1569-77.
11. Drake PM, Gunn MD, Charo IF, Tsou CL, Zhou Y, Huang L et al. Human placental cytotrophoblasts attract monocytes and CD56 (high) natural killer cells via the actions of monocytes inflammatory protein 1alpha. J Exp Med. 2001;193: 1199-1212.
12. King A, Jokhi PP, Burrows TD, Gardner L, Sharkey AM, Loke YW. Functions of human decidual NK cells. Am J Reprod Immunol. 1996; 35: 258-60.
13. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med. 2003; 198: 1201-12.
14. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001; 22: 633-40.
15. Hanna J, Bechtel P, Zhai Y, Youssef F, McLachlan K, Mandelboim O. Novel insights on human NK cells' immunological modalities revealed by gene expression profiling. J Immunol. 2004; 173: 6547-63.
16. Robertson MJ, Ritz J. Biology and clinical relevance of human natural killer cells. Blood. 1990; 76: 2421-38.
17. Dosiou C, Giudice LC. Natural Killer Cells in Pregnancy and Recurrent Pregnancy Loss: Endocrine and Immunologic Perspectives. Endocr Rev. 2005, 26: 44-62.
18. Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol. 1989; 143: 3183-91.
19. Le Bouteiller P and Piccini MP. Human NK cells in pregnant uterus: Why there? Am J Reprod Immunol. 2008; 59: 401-6.
20. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol. 2002; 2: 656-63.
21. Philippe LB, Julie T. Killers becomes builder during pregnancy. Nat Med. 2006; 12: 991-2.
22. Northern AL, Rutter SM, Peterson CM. Cyclic changes in the concentrations of peripheral blood immune cells during the normal menstrual cycle. Proc Soc Exp Biol Med. 1994; 207: 81-8.
23. Yovel G, Shakhar K, Ben-Eliyahu S. The effects of sex, menstrual cycle, and oral contraceptives on the number and activity of natural killer cells. Gynecol Oncol. 2001; 81:254-62.
24. Souza SS, Castro FA, Mendonca HC, Palma PV, Morais FR, Ferriani RA et al. Influence of menstrual cycle on NK activity. J Reprod Immunol. 2001; 50:151-9.
25. 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: 376-82.
26. Gregory CD, Lee H, Rees GB, Scott IV, Shah LP, Golding PR. Natural killer cells in normal pregnancy: analysis using monoclonal antibodies and single-cell cytotoxicity assays. Clin Exp Immunol. 1985; 62: 121-7.
27. Gregory CD, Lee H, Scott IV, Golding PR. Phenotypic heterogeneity and recycling capacity of natural killer cells in normal human pregnancy. J Reprod Immunol. 1987; 11: 135-45.
28. 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: 3054-63.
29. Sargent IL, Barzychowski AM, Redman CWG. NK cells and human pregnancy - an inflammatory view. Trends Immunol. 2006; 27: 399-04.
30. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod. 1991; 6: 791-8.
31. Kodama T, Hara T, Okamoto E, Kusunoki Y, Ohama K. Characteristic changes of large granular lymphocytes that strongly express CD56 in endometrium during the menstrual cycle and early pregnancy. Hum Reprod. 1998; 13: 1036-43.
32. Ponte M, Cantoni C, Biassoni R, Tradori-Cappai A, Bentivoglio G, Vitale C et al. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci USA. 1999; 96: 5674-9.
33. Henderson TA, Saunders PTK, King AM, Groome NP, Crichtley HOD. Steroid Receptor Expression in Uterine Natural Killer Cells. J Clin Endocrinol Metab. 2003; 88: 440-9.
34. Seppala M, Taylor RN, Koistinen H, Koistinen R, Milgrom E. Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr Rev. 2002; 23: 401-30.
35. 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: 3108-15.
36. Kitaya K, Nakayama T, Okubo T, Kuroboshi H, Fushiki S, Honjo H. Expression of macrophage inflammatory protein-1α in human endometrium: its role in endometrial recruitment of natural killer cells. J Clin Endocrinol Metab. 2003; 88: 1809-14.
37. Red-Horse K, Drake PM, Gunn MD, Fisher SJ. Chemokine ligand and receptor expression in the pregnant uterus: reciprocal patterns in complementary cell subsets suggest functional roles. Am J Pathol. 2001; 159: 2199-13.
38. Ancelin M, Buteau-Lozano H, Meduri G, Osborne-Pellegrin M, Sordello S, Plouet J et al. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc Natl Acad Sci USA. 2002; 99: 6023-8.
39. Popovici RM, Kao LC, Giudice LC. Discovery of new inducible genes in vitro decidualized human endometrial stromal cells using micro array technology. Endocrinology. 2000; 141: 3510-3.
40. Verma S, Hibby SE, Loke YW, King A. Human decidual natural killer cells express the receptor for IL-15 and respond to the cytokine interleukin 15. Biol Reprod. 2000; 62: 959-68.
41. Wu WX, Brooks J, Glasier AF, McNeilly AS. The relationship between decidualization and prolactin mRNA and production at different stages of human pregnancy. J Mol Endocrinol. 1995; 14: 255-61.
42. high natural killer cells of the human endometrium. J Clin Endocrinol Metab. 2002; 87: 2329-35.
43. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat rev Immunol. 2006; 6: 584-94.
44. Redline RW. Role of Uterine Natural Killer Cells and Interferon γ in Placental Development. J Exp Med. 2000; 192: F1-F4.
45. King A, Allan DS, Bowen M, Powis SJ, Joseph S, Verma S et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol. 2000; 30: 1623-31.
46. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I et al. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLOS Biol. 2006; 4:70-86.
47. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. 2006; 12:1065-74.
48. Hiby SE, Walker JJ, O'shaughnessy KM, Redman CW, Carrington M, Trowsdale J et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med. 2004; 200: 957-65.
49. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol. 2005; 5: 201-14.
50. Saito S, Nishikawa K, Morii T, Enomoto M, Narita N, Motoyoshi K et al. Cytokine production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Int Immunol. 1993; 5: 559-63.
51. King A. Uterine leukocytes and decidualization. Hum Reprod. 2004; 6:28-36.
52. Jokhi PP, Chumbley G, King A, Gardner L, Loke YW. 1993 Expression of the colony stimulating factor-1 receptor (c-fms product) by cells at the human uteroplacental interface. Lab Invest. 1993; 68: 308-20.
53. Yelavarthi KK, Hunt JS. Analysis of p60 and p80 tumor necrosis factor-α receptor messenger RNA and protein in human placentas. Am J Pathol. 1993; 143: 1131-41.
54. Peyman JA, Hammond GL. Localization of IFN γ receptor in first trimester placenta to trophoblasts but lack of stimulation of HLA-DRA, -DRB, or invariant chain mRNA expression by IFN. J Immunol. 1992; 149: 2675-80.
55. Tjwa M, Luttun A, Auteiro M, Carmeleit P. VEGF and PLGF : Two pleiotropic growth factors with distinct roles in development and homeostasis. Cell Tissue Res. 2003; 314: 5-14.
56. Saito S, Saito M, Enomoto M, Ito A, Motoyoshi K, Nakagawa T et al. Human macrophage colony-stimulating factor induces the differentiation of trophoblast. Growth Factors. 1993; 9: 11-19.
57. Kimber SJ. Leukaemia inhibitory factor in implantation and uterine biology. Reprod. 2005; 130: 131-45.
58. King A, Loke YW. Effect of IFN γ on killing of human trophoblast by decidual LAK cells. J Reprod Immunol. 1993; 23: 51-62.
59. Rabinovich GA, Baum LG, Tinari N, Paganelli R, Natoli C, Liu FT et al. Galectins and their ligands: amplifiers, silenc-ers or tuners of the inflammatory response? Trends Immunol. 2002; 23: 313-20.
60. Stirrat GM. Recurrent miscarriage. Lancet. 1990; 336:673-5.
61. Clifford K, Rai R, Watson H, Regan L. An informative protocol for the investigation of recurrent miscarriage: preliminary experience of 500 consecutive cases. Hum Reprod. 1994; 9: 1328-32.
62. Aokik.Kajiura S, Matsumoto Y, Ogasawara M, Okada S, Yagami Y, Gleicher N. Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet. 1995; 345: 1340-2.
63. Emmer PM, Nelen WL, Steegers EA, Hendriks JC, Veerhoek M, Joosten I. Peripheral natural killer cytotoxicity and CD56(pos)CD16(pos) cells increase during early pregnancy in women with a history of recurrent spontaneous abortion. Human Reprod. 2000; 15: 1163-9.
64. Ntrivalas EI, Kwak-Kim JY, Gilman-Sachs A, Chung-Bang H, Ng SC, Beaman KD et al. Status of peripheral blood natural killer cells in women with recurrent spontaneous abortions and infertility of unknown etiology. Hum Reprod. 2001; 16: 855-61.
65. Coulam CB, Goodman C, Roussev RG, Thomason E J, Beaman KD. Systemic CD56+ cells can predict pregnancy outcome. Am J Reprod Immunol. 1995; 33: 40-6.
66. Higuchi K, Aokik K, Kimbara T, Hosoin N, Yamamoto T, Okada H. Suppression of natural killer cell activity by monocytes following immunotherapy for recurrent spontaneous aborters. Am J Reprod Immunol. 1995; 33: 221-7.
67. Yamamoto T, Takahashi Y, Kase N, Mori H. Proportion of CD56[+]3[+] T cells in decidual and peripheral lymphocytes of normal pregnancy and spontaneous abortion with and without history of recurrent abortion. Am J Reprod Immunol. 1999; 42: 355-60.
68. Quack KC, Vassiliadou N, Pudney J, Anderson DJ, Hill JA. Leukocyte activation in the decidua of chromosomally normal and abnormal fetuses from women with recurrent abortion. Human Reprod. 2001; 16: 949-55.
69. Clifford K, Flanagan AM, Regan L. Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Human Reprod. 1999; 14: 2727-30.
70. Quenby S, Bates M, Doig T,Brewster J, Lewis-Jones DI, Johnson PM, Vince G. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Human Reproduction. 1999; 14:2386-91.
71. Quenby S, Vince G, Farquharson R, Aplin J. Recurrent miscarriage: a defect in nature's quality control? Human Reprod. 2002; 17: 1959-63.
72. Lachapelle MH, Miron P, Hemmings R, Roy DC. Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol. 1996; 156: 4027-34.
73. Emmer PM, Steegers EAP, Kerstens HMJ, Willianne JM, Nelen LDM, Boer K et al. Altered phenotype of HLA-G expressing trophoblast and decidual natural killer cells in pathological pregnancies. Human Reprod. 2002; 17: 1072-80.
74. Parham P. Killer cell immunoglobulin like receptor diversity: balancing signal in the natural killer cell response. Immunol Lett. 2004; 92:11-3.