Uterine leukocytes and decidualization

Human Reproduction Update

Volumn 6, Issue 1, 2000, Pages 28-36

  King, Ashley ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Decidua; Endometrium; Leukocytes; Menstruation; NK cells

Indexed keywords

LUTEINIZING HORMONE;

DECIDUA; DECIDUALIZATION; ENDOMETRIUM; FEMALE; HUMAN; LEUKOCYTE; LUTEINIZING HORMONE RELEASE; MENSTRUATION; NATURAL KILLER CELL; NIDATION; PREGNANCY; PRIORITY JOURNAL; REVIEW; STROMA CELL;

EID: 0033953884     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/6.1.28     Document Type: Review

References (98)

1. Arenas, M.J., Morris, R.G. and Wyllie, A.H. (1990) Apoptosis. The role of the endonuclease. Am. J. Pathol., 136, 593-604.
2. Ashkar, A.A. and Croy, B.A. (1999) Interferon-γ contributes to the normalcy of murine pregnancy. Biol. Reprod., 61, 493-502.
3. Beagley, K.W. and Husband, A.J. (1998) Intraepithelial lymphocytes: origins, distribution and function. Crit. Rev. Immunol., 18, 237-254.
4. Blagosklonny, M.V. (1999) A node between proliferation, apoptosis, and growth arrest. Bioessays, 21, 704-709.
5. Brar, A.K., Kessler, C.A., Meyer, A.J. et al. (1996) Retinoic acid suppresses in-vitro decidualization of human endometrial stromal cells. Mol. Hum. Reprod., 2, 185-193.
6. Braud, V.M., Allan, D.S.J., O'Callaghan, C.A. et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature, 391, 795-799.
7. Bulmer, J.N., Morrison, L., Longfellow, M. et al. (1991) Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum. Reprod., 6, 791-798.
8. Burrows, T.D., King, A. and Loke, Y.W. (1993) Expression of adhesion molecules by human decidual large granular lymphocytes. Cell. Immunol., 147, 81-94.
9. Burrows, T.D., King, A. and Loke, Y.W. (1995) The role of integrins in adhesion of decidual NK cells to extracellular matrix and decidual stromal cells. Cell. Immunol., 166, 53-61.
10. Carson, W. and Caligiuri, M. (1996) Natural killer cell subsets and development. Methods Companion Methods Enzymol., 9, 327-343.
11. Critchley, H.O.D., Wang, H., Jones, R.L. et al. (1998) Morphological and functional features of endometrial decidualization following long-term intrauterine levonorgestrel delivery. Hum. Reprod., 13, 1218-1224.
12. Croy, B.A. and Kiso, Y. (1993) Granulated metrial gland cells: a natural killer cell subset of the pregnant murine uterus. Micro. Res. Technol., 25, 189-200.
13. Croy, B.A., Luross, J.A., Guimond, M.-J. and Hunt, J.S. (1996/7) Uterine natural killer cells: insights into lineage relationships and functions from studies of pregnancies in mutant and transgenic mice. Nat. Immunity, 15, 22-33.
14. Croy, B.A., Whitelaw, P.F. and Engelhardt, H.E. (1998) The influences of immune cells on the success of pregnancy. In Bazer, F.W. (ed.), Endocrinology of Pregnancy. Humana Press, New Jersey, USA, pp. 229-289.
15. De Feo, V.J. (1967) Decidualization. In Cellular Biology of the Uterus. Meredith Publishing Company, New York, USA, pp. 191-290.
16. Deniz, G., Christmas, S.E. and Johnson, P.M. (1996) Soluble mediators and cytokines produced by human CD3-leucocyte clones from decidualized endometrium. Immunology, 87, 92-98.
17. Duboule, D. (1999) No milk today (my Hox have gone away). Proc. Natl Acad. Sci. USA, 96, 322-323.
18. Fehninger, T.A., Shah, M.H., Turner, M.J. et al. (1999) Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol., 162, 4511-4520.
19. Finn, C.A. (1996) Why do women menstruate? Historical and evolutionary review. Eur. J. Obstet. Gynecol. Reprod. Biol., 70, 3-8.
20. Finn, C.A. (1998) Menstruation: a nonadaptive consequence of uterine evolution. Q. Rev. Biol., 73, 163-173.
21. 2 dramatically enhances human endometrial stromal cell differentiation. Endocrinology, 134, 258-263.
22. Fujita, K., Nakayama, T., Takabatake, K. et al. (1998) Administration of thymocytes derived from non-pregnant mice induces an endometrial receptive stage and leukaemia inhibitory factor expression in the uterus. Hum. Reprod., 13, 2888-2894.
23. Fukui, A., Fujii, S., Yamaguchi, E. et al. (1999) Natural killer cell subpopulations and cytotoxicity for infertile patients undergoing in vitro fertilization. Am. J. Reprod. Immunol., 41, 413-422.
24. Gendron, R.L., Paradis, H., Hsieh-Li, H.M. et al. (1997) Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol. Reprod., 56, 1097-1105.
25. Goodger, A.M. and Rodgers, P.A.W. (1994) Endometrial endothelial cell proliferation during the menstrual cycle. Hum. Reprod., 9, 399-405.
26. Gui, Y., Zhang, J., Yuan, L. and Lessey, B.A. (1999) Regulation of HOXA-10 and its expression in normal and abnormal endometrium. Mol. Hum. Reprod., 5, 866-873.
27. Guimond, M.-J., Wang, B. and Croy, B.A. (1988) Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tgε26 mice. J. Exp. Med., 187, 217-223.
28. Halhali, A., Acker, G.M. and Garabedian, M. (1991) 1, 25-Dihydroxyvitamin D3 induces in vivo decidualization of rat endometrial cells. J. Reprod. Fertil., 91, 59-64.
29. Hameed, A., Fox, W.M., Kurman, R.J. et al. (1995) Perform expression in endometrium during the menstrual cycle. Int. J. Gyn. Pathol., 14, 143-150.
30. Hamilton, G.S., Lysiak, J.J., Han, V.K.M. and Lala, P.K. (1998) Autocrine-paracrine regulation of human trophoblast invasiveness by insulin-like growth factor (IGF)-II and IGF-binding protein (IGFBP)-1. Exp. Cell Res., 244, 147-156.
31. Hammer, A. and Dohr, G. (1999) Apoptotic nuclei within the uterine decidua of first trimester pregnancy arise from CD45 positive leukocytes. Am. J. Reprod. Immunol., 42, 88-94.
32. Hamperl, H. and Hellweg, G. (1958) Granular endometrial stromal cells. Obstet. Gynecol., 11, 379-387.
33. Head, J.R. (1996/7) Uterine natural killer cells during pregnancy in rodents. Nat. Immunol., 15, 7-21.
34. Hiby, S.E., King, A., Sharkey, A.M. and Loke, Y.W. (1997) Human uterine NK cells have a similar repertoire of killer inhibitory and activatory receptors to those found in blood, as demonstrated by RT-PCR and sequencing. Mol. Immunol., 34, 419-430.
35. Hill, J.A., Melling, G.C. and Johnson, P.M. (1995) Immunohistochemical studies of human uteroplacental tissues from first trimester spontaneous abortion. Am. J. Obstet. Gynecol., 173, 90-96.
36. + lymphocytes in an in vitro culture system. J. Clin. Endocrinol. Metab., 81, 1502-1507.
37. Isner, J.M. and Asahara, T. (1999) Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J. Clin. Invest., 103, 1231-1236.
38. Jones, R.K., Searle, R.F., Stewart, J.A.i. (1998) Apoptosis, bcl-2 expression, and proliferative activity in human endometrial stroma and endometrial granulated lymphocytes. Biol. Reprod., 58, 995-1002.
39. Kam, E.P.Y., Gardner, L., Loke, Y.W. and King, A. (1999) The role of trophoblast in the physiological change in decidual spiral arteries. Hum. Reprod., 14, 2131-2138.
40. + large granular lymphocytes in first-trimester human decidua are proliferating cells. Fertil. Steril., 71, 74-79.
41. Kim, J.J., Jaffe, R.C. and Fazleabas, A.T. (1998) Comparative studies on the in vitro decidualization process in the baboon (Papio anubis) and human. Biol. Reprod., 59, 160-168.
42. King, A. and Loke, Y.W. (1991) On the nature and function of human uterine granular lymphocytes. Immunol. Today, 12, 432-435.
43. King, A., Wellings, V., Gardner, L. and Loke, Y.W. (1989) Immunocytochemical characterisation of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum. Immunol., 24, 195-205.
44. ++ population. Dev. Immunol., 1, 169-190.
45. King, A., Gardner, L. and Loke, Y.W. (1996) Evaluation of oestrogen and progesterone receptor expression in uterine mucosal lymphocytes. Hum. Reprod., 11, 1079-1082.
46. King, A., Burrows, T. and Loke, Y.W. (1996/7) Human uterine natural killer cells. Nat. Immunity, 15, 41-52.
47. King, A., Burrows, T., Verma, S.I. (1998) Human uterine lymphocytes. Hum. Reprod. Update, 4, 480-485.
48. King, A., Gardner, L. and Loke, Y.W. (1999) Costimulation of human decidual natural killer cells by IL-2 and stromal cells. Hum. Reprod., 14, 656-663.
49. Komatsu, T., Konishi, I., Mandai, M. et al. (1998) Expression of class I human leukocyte antigen (HLA) and beta2-microglobulin is associated with decidualization of human endometrial stromal cells. Hum. Reprod., 13, 2246-2251.
50. Kruse, A., Merchant, M.J., Hallmann, R. and Butcher, E.C. (1999) Evidence of specialized leukocyte-vascular homing interactions at the maternal/fetal interface. Eur. J. Immunol., 29, 1116-1126.
51. Lachapelle, M.-H., Miron, P., Hemmings, R. and Roy, D.C. (1996) Endometrial T, B, and NK cells in patients with recurrent s pontaneous abortion. J. Immunol., 156, 4027-4034.
52. Lea, R.G., Underwood, J., Flanders, K.C. et al. (1995) A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor β-2-producing "suppressor cells" in uterine tissue near the placental attachment site. Am. J. Reprod. Immunol., 34, 52-64.
53. Lie, R.T., Rasmussen, S., Brunborg, H.I. (1998) Fetal and maternal contributions to risk of pre-eclampsia: population based study. Br. Med. J., 316, 1343-1347.
54. Lim, H., Paria, B.C., Das, S.K. et al. (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell, 91, 197-208.
55. 2-induced changes in the phenotype, morphology, and lytic activity of IL-2-activated natural killer cells. J. Immunol., 150, 3747-3754.
56. Loke, Y.W., King, A. and Burrows, T.D. (1995) Decidua in human implantation. Hum. Reprod., 10, 14-21.
57. Loke, Y.W. and King, A. (1995) Human Implantation: Cell Biology and Immunology. Cambridge University Press, Cambridge, UK.
58. Loke, YW and King, A. (1996) Immunology of human implantation: an evolutionary perspective. Hum. Reprod., 11, 283-286.
59. Loke, Y.W. and King, A. (2000) Immunological aspects of human implantation. Proceedings of Human Implantation: Recent Advances and Clinical Aspects. J. Reprod. Fertil., in press.
60. Ma, L., Benson, G.V., Lim, H. et al. (1998) Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in Mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev. Biol., 197, 141-154.
61. Maruyama, T., Makino, T., Sugi, T. et al. (1992) Flow cytometric analysis of immune cell populations in human decidua from various types of first trimester pregnancy. Hum. Immunol., 34, 212-218.
62. ++, CD3-, CD 16-large granular lymphocytes and endothelial cells in first trimester human decidua. Hum. Reprod., 8, 1203-1208.
63. Marx, L., Arck, P., Kapp, M. et al. (1999) Leukocyte populations, hormone receptors and apoptosis in eutopic and ectopic first trimester human pregnancies. Hum. Reprod., 14, 1111-1117.
64. Maslar, I.A. (1988) The progestational endometrium. Sem. Reprod. Endocrinol., 6, 115-128.
65. Massi, D., Susini, T., Paglierani, M. et al. (1995) Pregnancy-associated ectopic decidua. Acta Obstet. Gynecol. Scand., 74, 568-571.
66. Mingari, M.C., Vitale, C., Cantoni, C. et al. (1997) Interleukin-15-induced maturation of human natural killer cells from early thymic precursors: selective expression of CD94/NKG2-A as the only HLA class I-specific inhibitory receptor. Eur. J. Immunol., 27, 1374-1380.
67. Mizuno, K., Tanaka, T., Umesaki, N. and Ogita, S. (1998) Establishment and characterization of in vitro decidualization in normal human endometrial stromal cells. Osaka City Med. J., 44, 105-115.
68. Möller, M.J., Kammerer, R. and von Kleist, S. (1998) A distinct distribution of natural killer cell subgroups. Int. J. Cancer, 78, 533-538.
69. Negoescu, A., Guillermet, C., Lorimier, P. et al. (1998) TUNEL apoptotic cell detection in archived paraffin-embedded tissues. Biochemica, 3, 36-41.
70. Osteen, K.G. (1998) The endocrinology of uterine decidualization. In Bazer, F.W. (ed.), Endocrinology of Pregnancy. Humana Press, New Jersey, USA, pp.541-553.
71. Pace, D., Morrison, L. and Bulmer, J.N. (1989) Proliferative activity in endometrial stromal granulocytes throughout menstrual cycle and early pregnancy. J. Clin. Pathol., 42, 35-39.
72. + CD16-CD3-large granular lymphocytes generated from human duodenal mucosa. Immunology, 79, 498-505.
73. Piccinni, M.-P., Beloni, L., Livi, C. et al. (1998) Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nature Med., 4, 1020-1024.
74. Pijnenborg, R. (1998) The human decidua as a passage-way for trophoblast invasion. A review. Troph. Res., 11, 229-241.
75. Robb, L., Li, R., Hartley, L. et al. (1998) Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nature Med., 4, 303-308.
76. Robertson, W.B. (1987) Pathology of the pregnant uterus. In Fox, H. (ed.), Obstetrical and Gynecological Pathology. Churchill Livingstone, Edinburgh, UK, pp. 1149-1175.
77. Rodgers, P.A.W., Lederman, F. and Taylor, N. (1998) Endometrial microvascular growth in normal and dysfunctional states. Hum. Reprod. Update, 4, 503-508.
78. 3 induction in myeloid leukemic cells. Mol. Cell. Biol., 18, 1911-1918.
79. Sharkey, A.M., King, A., Clark, D.E. et al. (1999) Localization of leukemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol. Reprod., 60, 355-364.
80. Sobis, H., Waer, M. and Vandeputte, M. (1996) Normal and malignant trophoblasts do not recruit granulated metrial gland cells. Tumor Biol., 17, 13-19.
81. Song, J.Y., Russell, P., Markham, R. et al. (1996) Effect of high dose progestogens on white cells and necrosis in human endometrium. Hum. Reprod., 11, 1713-1718.
82. Spornitz, U.M. (1992) The functional morphology of the human endometrium and decidua. Adv. Anat. Embryol. Cell Biol., 124, 1-99.
83. Stallmach, T., Ehrenstein, T., Isenmann, S. et al. (1995) The role of perform expression by granular metrial gland cells in pregnancy. Eur. J. Immunol., 25, 3342-3348.
84. Starkey, P.M., Sargent, I.L. and Redman, C.W.G. (1988) Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology, 65, 129-134.
85. Stewart, C.L. and Cullinan, E.B. (1997) Preimplantation development of the mammalian embryo and its regulation by growth factors. Dev. Genet., 21, 91-101.
86. Stewart, J.A., Bulmer, J.N. and Murdoch, A.P. (1998) Endometrial leucocytes: expression of steroid hormone receptors. J. Clin. Pathol., 51, 121-126.
87. Takabatake, K., Fujiwara, H., Goto, Y., Nakayama, T., Higuchi, T., Fujita, J., Maeda, M. and Mori, T. (1997) Splenocytes in early pregnancy promote embryo implantation by regulating endometrial differentiation in mice. Hum. Reprod., 12, 2102-2107.
88. Tang, B., Guller, S. and Gurpide, E. (1993) Cyclic adenose 3′, 5′-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium. Endocrinology, 133, 2197-2203.
89. Taylor, H.S., Arici, A., Olive, D. and Igarashi, P. (1998) HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest., 101, 1379-1384.
90. + NK cells in the endometrium of women suffering spontaneous early pregnancy loss. Hum. Reprod., 11, 1569-1574.
91. Vassiliadou, N. and Bulmer, J.N. (1998a) Characterization of tubal and decidual leukocyte populations in ectopic pregnancy: evidence that endometrial granulated lymphocytes are absent from the tubal implantation site. Fertil. Steril., 69, 760-767.
92. Vassiliadou, N. and Bulmer, J.N. (1998b) Characterization of endometrial T lymphocyte subpopulations in spontaneous early pregnancy loss. Hum. Reprod., 13, 44-47.
93. + lymphocytes on killing of NK-and LAK-sensitive targets. Biol. Reprod., 58, 982-987.
94. Vassiliadou, N., Searle, R.F. and Bulmer, J.N. (1999) Elevated expression of activation molecules by decidual lymphocytes in women suffering spontaneous early pregnancy loss. Hum. Reprod., 14, 1194-1200.
95. Verma, S., King, A. and Loke, Y.W. (1997) Expression of killer-cell inhibitory receptors (KIR) on human uterine NK cells. Eur. J. Immunol., 27, 979-983.
96. Vicovac, J.M., Starkey, P.M. and Aplin, J.D. (1994) Effect of cytokines on prolactin production by human decidual stromal cells in culture: studies using cells freed of bone marrow-derived contaminants. J. Clin. Endocrinol. Metab., 79, 1877-1892.
97. Waldmann, T.A. and Tagaya, Y. (1999) The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu. Rev. Immunol., 17, 19-49.
98. Ye, W., Zheng, L.-M., Young, J.D-E. and Liu, C.-C. (1996) The involvement of interleukin (IL)-15 in regulating the differentiation of granulated metrial gland cells in mouse pregnant uterus. J. Exp. Med., 184, 2405-2410.