Human uterine natural killer cells: A reappraisal

Molecular Immunology

Volumn 42, Issue 4 SPEC. ISS., 2005, Pages 511-521

  Bulmer, Judith N ^a,b   Lash, Gendie E ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

Decidua; Endometrial granulated lymphocyte; Endometrium; Pregnancy; Spiral artery; Trophoblast invasion; Uterine NK cell

Indexed keywords

GAMMA INTERFERON;

CYTOKINE PRODUCTION; DECIDUA; HUMAN; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REVIEW; TROPHOBLAST; UTERINE BLOOD VESSEL; UTERUS;

EID: 10644246068     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2004.07.035     Document Type: Short Survey

References (101)

1. A.A. Ashkar, J.P. Di Santo, and B.A. Croy Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy J. Exp. Med. 192 2000 259 270
2. G.W. Bartelemez, G.W. Corner, and G.G. Hartman Cyclic changes in the endometrium of the rhesus monkey (Macaca mulatto) Contrib. Embryol. Carnegie Inst. Wash. 34 1951 99 144
3. S. Bauer, J. Pollheimer, J. Hartmann, P. Husslein, J.D. Aplin, and M. Knofler Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures J. Clin. Endocrinol. Metab. 89 2004 812 822
4. J.N. Bulmer, and C.A. Sunderland Immunohistological characterization of lymphoid cell populations in the early human placental bed Immunology 52 1984 349 357
5. J.N. Bulmer, J. Smith, L. Morrison, and M. Wells Maternal and fetal cellular relationships in the human placental basal plate Placenta 9 1988 237 246
6. J.N. Bulmer, L. Morrison, M. Longfellow, A. Ritson, and D. Pace Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies Hum. Reprod. 6 1991 791 798
7. T.D. Burrows, A. King, and Y.W. Loke The role of integrins in adhesion of decidual NK cells to extracellular matrix and decidual stromal cells Cell. Immunol. 166 1995 53 61
8. J.J. Campbell, S. Qin, D. Unutmaz, D. Soler, K.E. Murphy, M.R. Hodge, L. Wu, and E.C. Butcher Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire J. Immunol. 166 2001 6477 6482
9. R.R. Cardell, F.L. Hisaw, and A.B. Dawson The fine structure of granular cells in the uterine endometrium of the rhesus monkey (Macaca mulatto) with a discussion of the possible function of these cells in relaxin secretion Am. J. Anat. 124 1969 307 340
10. J.E. Cartwright, L.C. Kenny, P.R. Dash, I.P. Crocker, J.D. Aplin, P.N. Baker, and G.S. Whitley Trophoblast invasion of spiral arteries: a novel in vitro model Placenta 23 2002 232 235
11. S. Chantakru, C. Miller, L.E. Roach, W.A. Kuziel, N. Maeda, W.C. Wang, S.S. Evans, and B.A. Croy Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy J. Immunol. 168 2002 22 28
12. S.E. Christmas, J.N. Bulmer, A. Meager, and P.M. Johnson Phenotypic and functional analysis of human CD3- decidual leucocyte clones Immunology 71 1990 182 189
13. G. Chumbley, A. King, K. Robertson, N. Holmes, and Y.W. Loke Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells Cell. Immunol. 155 1994 312 322
14. D.A. Clark, K.C. Flanders, D. Banwatt, W. Millar-Book, J. Manuel, J. Stedronska-Clark, and B. Rowley Murine pregnancy decidua produces a unique immunosuppressive molecule related to transforming growth factor beta-2 J. Immunol. 144 1990 3008 3014
15. D.A. Clark, G. Vince, K.C. Flanders, H. Hirte, and P. Starkey CD56+ lymphoid cells in human first trimester pregnancy decidua as a source of novel transforming growth factor-beta 2-related immunosuppressive factors Hum. Reprod. 9 1994 2270 2277
16. M.A. Cooper, T.A. Fehniger, and M.A. Caligiuri The biology of human natural killer-cell subsets Trends Immunol. 22 2001 633 640
17. C.M. Craven, T. Morgan, and K. Ward Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts Placenta 19 1998 241 252
18. F.D. Dallenbach, and G. Dallenbach-Hellweg Immunohistolgische untersuchungen zur lakalisation des relaxius in menschlicher placenta und decidua Virch. Arch. Path. Anat. 337 1964 301 316
19. G. Dallenbach-Hellweg Histopathology of the Endometrium 1987 Springer-Verlag Berlin
20. G. Dallenbach-Hellweg, and G. Nette Morphological and histochemical observations on trophoblast and decidua of the basal plate of the human placenta at term J. Anat. 115 1964 309 326
21. B. Disep, B.A. Innes, E. Ball, S.C. Robson, and J.N. Bulmer Quantitative assessment of apoptosis in the placenta bed of normal and abnormal pregnancies Placenta 24 2003 A.16
22. B.L. Drake, and J.R. Head Murine trophoblast can be killed by lymphokine-activated killer cells J. Immunol. 143 1989 9 14
23. C. Dunk, M. Shams, S. Nijjar, M. Rhaman, Y. Qiu, B. Bussolati, and A. Ahmed Angiopoietin-1 and angiopoietin-2 activate trophoblast Tie-2 to promote growth and migration during placental development Am. J. Pathol. 156 2000 2185 2199
24. H. Engelhardt, and G.J. King Uterine natural killer cells in species with epitheliochorial placentation Nat. Immun. 15 1996/1997 53 69
25. B.L. Ferry, P.M. Starkey, I.L. Sargent, G.M. Watt, M. Jackson, and C.W. Redman Cell populations in the human early pregnancy decidua: natural killer activity and response to interleukin-2 of CD56-positive large granular lymphocytes Immunology 70 1990 446 452
26. B.L. Ferry, I.L. Sargent, P.M. Starkey, and C.W. Redman Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from human early pregnancy decidua Cell. Immunol. 132 1991 140 149
27. C.H. Graham, I. Connelly, J.R. MacDougall, R.S. Kerbel, W.G. Stetler-Stevenson, and P.K. Lala Resistance of malignant trophoblast cells to both the anti-proliferative and anti-invasive effects of transforming growth factor-beta Exp. Cell. Res. 214 1994 93 99
28. O. Gubbay, H.O. Critchley, J.M. Bowen, A. King, and H.N. Jabbour Prolactin induces ERK phosphorylation in epithelial and CD56(+) natural killer cells of the human endometrium J. Clin. Endocrinol. Metab. 87 2002 2329 2335
29. L. Gudelj, G. Deniz, D. Rukavina, P.M. Johnson, and S.E. Christmas Expression of functional molecules by human CD3- decidual granular leucocyte clones Immunology 87 1996 609 615
30. L. Gudelj, S.E. Christmas, G. Laskarin, P.M. Johnson, E.R. Podack, and D. Rukavina Membrane phenotype and expression of perforin and serine esterases by CD3- peripheral blood and decidual granular lymphocyte-derived clones Am. J. Reprod. Immunol. 38 1997 162 167
31. M.J. Guimond, B. Wang, and B.A. Croy 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. 187 1998 217 223
32. H. Haller, O. Radillo, D. Rukavina, F. Tedesco, G. Candussi, O. Petrovic, and L. Randic An immunohistochemical study of leucocytes in human endometrium, first and third trimester basal decidua J. Reprod. Immunol. 23 1993 41 49
33. H. Haller, F. Tedesco, D. Rukavina, O. Radillo, L. Gudelj, and A.E. Beer Decidual-trophoblast interactions: decidual lymphoid cell populations in basal and parietal decidua J. Reprod. Immunol. 28 1995 165 171
34. A. Hammer, and G. Dohr Apoptotic nuclei within the uterine decidua of first trimester pregnancy arise from CD45 positive leukocytes Am. J. Reprod. Immunol. 42 1999 88 94
35. H. Hamperl, and G. Hellweg Granular endometrial stroma cells Obstet. Gynecol. 11 1958 379 387
36. J. Hanna, O. Wald, D. Goldman-Wohl, D. Prus, G. Markel, R. Gazit, G. Katz, R. Haimov-Kochman, N. Fujii, S. Yagel, A. Peled, and O. Mandelboim CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells Blood 102 2003 1569 1577
37. T.A. Henderson, P.T. Saunders, A. Moffett-King, N.P. Groome, and H.O. Critchley Steroid receptor expression in uterine natural killer cells J. Clin. Endocrinol. Metab. 88 2003 440 449
38. E. Jauniaux, A.L. Watson, J. Hempstock, Y.P. Bao, J.N. Skepper, and G.J. Burton Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure Am. J. Pathol. 157 2000 2111 2122
39. P.P. Jokhi, A. King, A.M. Sharkey, S.K. Smith, and Y.W. Loke Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction J. Immunol. 153 1994 4427 4435
40. P.P. Jokhi, A. King, and Y.W. Loke Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface Cytokine 9 1997 126 137
41. R.K. Jones, J.N. Bulmer, and R.F. Searle Cytotoxic activity of endometrial granulated lymphocytes during the menstrual cycle in humans Biol. Reprod. 57 1997 1217 1222
42. R.K. Jones, R.F. Searle, J.A. Stewart, S. Turner, and J.N. Bulmer Apoptosis, bcl-2 expression, and proliferative activity in human endometrial stroma and endometrial granulated lymphocytes Biol. Reprod. 58 1998 995 1002
43. R.K. Jones, R.F. Searle, and J.N. Bulmer Apoptosis and bcl-2 expression in normal human endometrium, endometriosis and adenomyosis Hum. Reprod. 13 1998 3496 3502
44. E.P. Kam, L. Gardner, Y.W. Loke, and A. King The role of trophoblast in the physiological change in decidual spiral arteries Hum. Reprod. 14 1999 2131 2138
45. B.A. Kazzaz Specific endometrial granular cells. A semiquantitative study Eur. J. Obstet. Gynecol. 3 1972 77 84
46. T.Y. Khong Immunohistologic study of the leukocytic infiltrate in maternal uterine tissues in normal and preeclamptic pregnancies at term Am. J. Reprod. Immunol. Microbiol. 15 1987 1 8
47. A. King, V. Wellings, L. Gardner, and Y.W. Loke Immunocytochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle Hum. Immunol. 24 1989 195 205
48. A. King, C. Birkby, and Y.W. Loke Early human decidual cells exhibit NK activity against the K562 cell line but not against first trimester trophoblast Cell. Immunol. 118 1989 337 344
49. A. King, N. Balendran, P. Wooding, N.P. Carter, and Y.W. Loke CD3- leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56++ population Dev. Immunol. 1 1991 169 190
50. A. King, P. Wooding, L. Gardner, and Y.W. Loke Expression of perforin, granzyme A and TIA-1 by human uterine CD56+ NK cells implies they are activated and capable of effector functions Hum. Reprod. 8 1993 2061 2067
51. A. King, L. Gardner, and Y.W. Loke Evaluation of oestrogen and progesterone receptor expression in uterine mucosal lymphocytes Hum. Reprod. 11 1996 1079 1082
52. A. King, L. Gardner, and Y.W. Loke Co-stimulation of human decidual natural killer cells by interleukin-2 and stromal cells Hum. Reprod. 14 1999 656 663
53. A. King, S.E. Hiby, L. Gardner, S. Joseph, J.M. Bowen, S. Verma, T.D. Burrows, and Y.W. Loke Recognition of trophoblast HLA class I molecules by decidual NK cell receptors - a review Placenta 21 2000 S81 S85
54. K. Kitaya, J. Yasuda, I. Yagi, Y. Tada, S. Fushiki, and H. Honjo IL-15 expression at human endometrium and decidua Biol. Reprod. 63 2000 683 687
55. K. Kitaya, J. Yasuda, T. Nakayama, S. Fushiki, and H. Honjo Effect of female sex steroids on human endometrial CD16neg CD56bright natural killer cells Fertil. Steril. 79 2003 730 734
56. K. Kusakabe, T. Okada, F. Sasaki, and Y. Kiso Cell death of uterine natural killer cells in murine placenta during placentation and preterm periods J. Vet. Med. Sci. 61 1999 1093 1100
57. R.G. Lea, J. Underwood, K.C. Flanders, H. Hirte, D. Banwatt, S. Finotto, I. Ohno, S. Daya, C. Harley, and M. Michel A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor beta-2-producing suppressor cells in uterine tissue near the placental attachment site Am. J. Reprod. Immunol. 34 1995 52 64
58. X.F. Li, D.S. Charnock-Jones, E. Zhang, S. Hiby, S. Malik, K. Day, D. Licence, J.M. Bowen, L. Gardner, A. King, Y.W. Loke, and S.K. Smith Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells J. Clin. Endocrinol. Metab. 86 2001 1823 1834
59. K. Marzusch, P. Ruck, A. Geiselhart, R. Handgretinger, J.A. Dietl, E. Kaiserling, H.P. Horny, G. Vince, and C.W. Redman Distribution of cell adhesion molecules on CD56++, CD3-, CD16- large granular lymphocytes and endothelial cells in first-trimester human decidua Hum. Reprod. 8 1993 1203 1208
60. K. Nishikawa, S. Saito, T. Morii, K. Hamada, H. Ako, N. Narita, M. Ichijo, M. Kurahayashi, and K. Sugamura Accumulation of CD16-CD56+ natural killer cells with high affinity interleukin 2 receptors in human early pregnancy decidua Int. Immunol. 3 1991 743 750
61. S. Okada, H. Okada, M. Sanezumi, T. Nakajima, K. Yasuda, and H. Kanzaki Expression of interleukin-15 in human endometrium and decidua Mol. Hum. Reprod. 6 2000 75 80
62. H.A. Otun, G.E. Lash, J.N. Bulmer, R.F. Searle, and S.C. Robson Inhibition of first trimester human extravillous trophoblast invasion by TNF-α and IFN-γ Placenta 24 2003 A.67
63. H.A. Otun, G.E. Lash, B. Innes, J.N. Bulmer, R.F. Searle, and S.C. Robson Regulation of trophoblast invasion by TGF-β: role of apoptosis and proliferation J. Soc. Gynecol. Investig. 11 2004 221a
64. V.A. Paffaro Jr., M.C. Bizinotto, P.P. Joazeiro, and A.T. Yamada Subset classification of mouse uterine natural killer cells by DBA lectin reactivity Placenta 24 2003 479 488
65. S. Peel, I.J. Stewart, and D. Bulmer Experimental evidence for the bone marrow origin of granulated metrial gland cells of the mouse uterus Cell Tissue Res. 233 1983 647 656
66. R.J. Phillips, B.A. Innes, R.F. Searle, J.N. Bulmer, and S.C. Robson Use of laser capture microdissection and RT-PCR to study gene expression in heterogeneous, differentiating trophoblast populations J. Soc. Gynecol. Investig. 10 2003 398a
67. R. Pijnenborg, J.M. Bland, W.B. Robertson, and I. Brosens Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy Placenta 4 1983 397 413
68. Pongcharoen, S., Bulmer, J.N., Searle, R.F., in press. No evidence for apoptosis of decidual leucocytes in normal and molar pregnancy; implications for immune privilege. Clin. Exp. Immunol.
69. L. Rieger, U. Kammerer, J. Hofmann, M. Sutterlin, and J. Dietl Choriocarcinoma cells modulate the cytokine production of decidual large granular lymphocytes in coculture Am. J. Reprod. Immunol. 46 2001 137 143
70. A. Ritson, and J.N. Bulmer Endometrial granulocytes in human decidua react with a natural-killer (NK) cell marker, NKH1 Immunology 62 1987 329 331
71. A. Ritson, and J.N. Bulmer Extraction of leucocytes from human deciduas. A comparison of dispersal techniques J. Immunol. Meth. 104 1987 231 236
72. A. Ritson, and J.N. Bulmer Isolation and functional studies of granulated lymphocytes in first trimester human decidua Clin. Exp. Immunol. 77 1989 263 268
73. W.B. Robertson The Endometrium 1981 Butterworths Press London
74. E.E. Rosmaraki, I. Douagi, C. Roth, F. Colucci, A. Cumano, and J.P. Di Santo Identification of committed NK cell progenitors in adult murine bone marrow Eur. J. Immunol. 31 2001 1900 1909
75. N. Rouas-Freiss, R.M. Goncalves, C. Menier, J. Dausset, and E.D. Carosella Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis Proc. Natl. Acad. Sci. U.S.A. 94 1997 11520 11525
76. P. Ruck, K. Marzusch, E. Kaiserling, H.P. Horny, J. Dietl, A. Geiselhart, R. Handgretinger, and C.W. Redman Distribution of cell adhesion molecules in decidua of early human pregnancy. An immunohistochemical study Lab. Invest. 71 1994 94 101
77. P.J. Scaife, R.F. Searle, S.C. Robson, B.A. Innes, and J.N. Bulmer A comparison of cytotoxic decidual leucocyte populations in early and late pregnancy J. Soc. Gynecol. Investig. 10 2003 360
78. P.J. Scaife, R.F. Searle, S.C. Robson, B.A. Innes, and J.N. Bulmer cytokine production by CD8+ decidual leucocytes in early pregnancy J. Soc. Gynecol. Investig. 11 2004 285A
79. R.F. Searle, R.K. Jones, and J.N. Bulmer Phenotypic analysis and proliferative responses of human endometrial granulated lymphocytes during the menstrual cycle Biol. Reprod. 60 1999 871 878
80. A.P. Sindram-Trujillo, S.A. Scherjon, P.P. van Hulst-van Miert, J.J. van Schip, H.H. Kanhai, D.L. Roelen, and F.H. Claas Differential distribution of NK cells in decidua basalis compared with decidua parietalis after uncomplicated human term pregnancy Hum. Immunol. 64 2003 921 929
81. I.I. Slukvin, D.P. Lunn, D.I. Watkins, and T.G. Golos Placental expression of the nonclassical MHC class I molecule Mamu-AG at implantation in the rhesus monkey Proc. Natl. Acad. Sci. U.S.A. 97 2000 9104 9109
82. I.I. Slukvin, D.I. Watkins, and T.G. Golos Phenotypic and functional characterization of rhesus monkey decidual lymphocytes: rhesus decidual large granular lymphocytes express CD56 and have cytolytic activity J. Reprod. Immunol. 50 2001 57 79
83. I.I. Slukvin, E.E. Breburda, and T.G. Golos Dynamic changes in primate endometrial leukocyte populations: differential distribution of macrophages and natural killer cells at the rhesus monkey implantation site and in early pregnancy Placenta 25 2004 297 307
84. L.J. Smith Metrial gland and other glycogen containing cells in the mouse uterus following mating and through implantation of the embryo Am. J. Anat. 119 1966 15 23
85. U.M. Spornitz The functional morphology of the human endometrium and decidua Adv. Anat. Embryol. Cell Biol. 124 1992 1 99
86. I. Stewart, and D.D. Mukhtar The killing of mouse trophoblast cells by granulated metrial gland cells in vitro Placenta 9 1988 417 425
87. I.J. Stewart Granulated metrial gland cells in minor species J. Reprod. Immunol. 40 1998 129 146
88. I.J. Stewart Mouse granulated metrial gland cells require contact with stromal cells to maintain viability J. Anat. 197 2000 495 502
89. J.A. Stewart, J.N. Bulmer, and A.P. Murdoch Endometrial leucocytes: expression of steroid hormone receptors J. Clin. Pathol. 51 1998 121 126
90. M.S. Torres, C.I. Ace, and W.C. Okulicz Assessment and application of laser microdissection for analysis of gene expression in the rhesus monkey endometrium Biol. Reprod. 67 2002 1067 1072
91. A. Trundley, and A. Moffett Human uterine leukocytes and pregnancy Tissue Antigens 63 2004 1 12
92. A. van der Meer, H.G. Lukassen, M.J. van Lierop, F. Wijnands, S. Mosselman, D.D. Braat, and I. Joosten Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells Mol. Hum. Reprod. 10 2004 189 195
93. M.L. Vargas, J.L. Santos, C. Ruiz, M.J. Montes, P. Aleman, C. Garcia-Tortosa, and E. Garcia-Olivares Comparison of the proportions of leukocytes in early and term human decidua Am. J. Reprod. Immunol. 29 1993 135 140
94. N. Vassiliadou, and J.N. Bulmer 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 1998 760 767
95. N. Vassiliadou, and J.N. Bulmer Expression of CD69 activation marker by endometrial granulated lymphocytes throughout the menstrual cycle and in early pregnancy Immunology 94 1998 368 375
96. N. Vassiliadou, and J.N. Bulmer Functional studies of human decidua in spontaneous early pregnancy loss: effect of soluble factors and purified CD56+ lymphocytes on killing of natural killer- and lymphokine-activated killer-sensitive targets Biol. Reprod. 58 1998 982 987
97. N. Vassiliadou, R.F. Searle, and J.N. Bulmer Immunoregulatory activity of decidua in spontaneous early pregnancy loss Hum. Reprod. 14 1999 2252 2256
98. U. von Rango, I. Classen-Linke, S. Kertschanska, B. Kemp, and H.M. Beier Effects of trophoblast invasion on the distribution of leukocytes in uterine and tubal implantation sites Fertil. Steril. 76 2001 116 124
99. U. von Rango, I. Classen-Linke, G. Raven, F. Bocken, and H.M. Beier Cytokine microenvironments in human first trimester decidua are dependent on trophoblast cells Fertil. Steril. 79 2003 1176 1186
100. T.G. Wegmann, H. Lin, L. Guilbert, and T.R. Mosmann Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today 14 1993 353 356
101. P. Weill Les cellules granuleuses des muqueuses intestinale et uterine Arch. Anat. Microsc. 17 1921 77 82